GATA6 and FOXA2 regulate wnt6 expression during extraembryonic endoderm formation

Stem Cells and Development

Volumn 21, Issue 17, 2012, Pages 3220-3232

  Hwang, Jason T K ^a   Kelly, Gregory M ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BUCLADESINE; HEPATOCYTE NUCLEAR FACTOR 3BETA; MESSENGER RNA; RETINOIC ACID; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR GATA 6; WNT6 PROTEIN;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; GENE EXPRESSION REGULATION; GENE SWITCHING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARIETAL EXTRAEMBRYONIC ENDODERM; PRIMITIVE EXTRAEMBRYONIC ENDODERM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; WNT SIGNALING PATHWAY;

ANIMALS; BUCLADESINE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; CLONING, MOLECULAR; ENDODERM; EPITHELIAL-MESENCHYMAL TRANSITION; GATA6 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 3-BETA; MICE; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; RNA, MESSENGER; TCF TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TRETINOIN; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84869040727     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0492     Document Type: Article

References (80)

1. Katoh Y and M Katoh. (2005). Identification and characterization of rat Wnt6 and Wnt10a genes in silico. Int J Mol Med 15:527-531.
2. Koutsourakis M, A Langeveld, R Patient, R Beddington and F Grosveld. (1999). The transcription factor GATA6 is essential for early extraembryonic development. Development 126:723-732. (Pubitemid 29106179)
3. Chazaud C, Y Yamanaka, T Pawson and J Rossant. (2006). Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 10:615-624.
4. Rossant J and PP Tam. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136:701-713.
5. Tam PP and DA Loebel. (2007). Gene function in mouse embryogenesis: get set for gastrulation. Nat Rev Genet 8: 368-381. (Pubitemid 46625808)
6. Strickland S and V Mahdavi. (1978). The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell 15:393-403. (Pubitemid 9052408)
7. Strickland S, KK Smith and KR Marotti. (1980). Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell 21:347-355. (Pubitemid 10047088)
8. Su D and LJ Gudas. (2008). Gene expression profiling elucidates a specific role for RARgamma in the retinoic acidinduced differentiation of F9 teratocarcinoma stem cells. Biochem Pharmacol 75:1129-1160.
9. Eifert C, N Sangster-Guity, LM Yu, SV Chittur, AV Perez, JA Tine and PJ McCormick. (2006). Global gene expression profiles associated with retinoic acid-induced differentiation of embryonal carcinoma cells. Mol Reprod Dev 73:796-824. (Pubitemid 43825286)
10. Krawetz R, MJ MacKenzie, Q Sun, PA Walton and GM Kelly. (2006). Galpha13 activation rescues moesin-depletion induced apoptosis in F9 teratocarcinoma cells. Exp Cell Res 312:3224-3240. (Pubitemid 44380228)
11. Verheijen MH, RM Wolthuis, JL Bos and LH Defize. (1999). The Ras/Erk pathway induces primitive endoderm but prevents parietal endoderm differentiation of F9 embryonal carcinoma cells. J Biol Chem 274:1487-1494.
12. Krawetz R and GM Kelly. (2009). Coordinate Galpha13 and Wnt6-beta-catenin signaling in F9 embryonal carcinoma cells is required for primitive endoderm differentiation. Biochem Cell Biol 87:567-580.
13. Krawetz R and GM Kelly. (2008). Wnt6 induces the specification and epithelialization of F9 embryonal carcinoma cells to primitive endoderm. Cell Signal 20:506-517.
14. Liu T, YN Lee, CC Malbon and HY Wang. (2002). Activation of the beta-catenin/Lef-Tcf pathway is obligate for formation of primitive endoderm by mouse F9 totipotent teratocarcinoma cells in response to retinoic acid. J Biol Chem 277:30887-30891. (Pubitemid 34970789)
15. Sugimura R and L Li. (2010). Noncanonical Wnt signaling in vertebrate development, stem cells, and diseases. Birth Defects Res C Embryo Today 90:243-256.
16. Rao TP and M Kuhl. (2010). An updated overview on Wnt signaling pathways: a prelude for more. Circ Res 106: 1798-1806.
17. Cadigan KM and M Peifer. (2009). Wnt signaling from development to disease: insights from model systems. Cold Spring Harb Perspect Biol 1:a002881.
18. MacDonald BT, K Tamai and X He. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9-26.
19. Kemp C, E Willems, S Abdo, L Lambiv and L Leyns. (2005). Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev Dyn 233:1064-1075. (Pubitemid 40853485)
20. Maretto S, M Cordenonsi, S Dupont, P Braghetta, V Broccoli, AB Hassan, D Volpin, GM Bressan and S Piccolo. (2003). Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A 100:3299-3304. (Pubitemid 36356577)
21. Barker N. (2008). The canonical Wnt/beta-catenin signalling pathway. Methods Mol Biol 468:5-15.
22. Wend P, JD Holland, U Ziebold and W Birchmeier. (2010). Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol 21:855-863.
23. Lucero OM, DW Dawson, RT Moon and AJ Chien. (2010). A re-evaluation of the ''oncogenic'' nature of Wnt/beta-catenin signaling in melanoma and other cancers. Curr Oncol Rep 12:314-318.
24. Ying Y and Q Tao. (2009). Epigenetic disruption of the WNT/beta-catenin signaling pathway in human cancers. Epigenetics 4:307-312.
25. Kohn AD and RT Moon. (2005). Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium 38: 439-446. (Pubitemid 41283282)
26. Strutt DI, U Weber and M Mlodzik. (1997). The role of RhoA in tissue polarity and Frizzled signalling. Nature 387:292-295. (Pubitemid 27220765)
27. Wallingford JB. (2006). Planar cell polarity, ciliogenesis and neural tube defects. Hum Mol Genet 15 Spec No. 2: R227-R234. (Pubitemid 44446798)
28. Boutros M, N Paricio, DI Strutt and M Mlodzik. (1998). Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94:109-118. (Pubitemid 28347474)
29. Kuhl M, LC Sheldahl, CC Malbon and RT Moon. (2000). Ca(2 +) /calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J Biol Chem 275:12701-12711. (Pubitemid 30241421)
30. Westfall TA, R Brimeyer, J Twedt, J Gladon, A Olberding, M Furutani-Seiki and DC Slusarski. (2003). Wnt-5/pipetail functions in vertebrate axis formation as a negative regulator of Wnt/beta-catenin activity. J Cell Biol 162:889-898. (Pubitemid 37087728)
31. Ma L and HY Wang. (2007). Mitogen-activated protein kinase p38 regulates the Wnt/cyclic GMP/Ca2 + non-canonical pathway. J Biol Chem 282:28980-28990. (Pubitemid 47606074)
32. Lee YN, CC Malbon and HY Wang. (2004). G alpha 13 signals via p115RhoGEF cascades regulating JNK1 and primitive endoderm formation. J Biol Chem 279:54896-54904. (Pubitemid 40053236)
33. Bikkavilli RK,ME Feigin and CCMalbon. (2008). p38mitogenactivated protein kinase regulates canonical Wnt-beta-catenin signaling by inactivation ofGSK3beta. JCell Sci 121:3598-3607.
34. Capo-Chichi CD, ME Rula, JL Smedberg, L Vanderveer, MS Parmacek, EE Morrisey, AK Godwin and XX Xu. (2005). Perception of differentiation cues by GATA factors in primitive endoderm lineage determination of mouse embryonic stem cells. Dev Biol 286:574-586. (Pubitemid 41443294)
35. Fujikura J, E Yamato, S Yonemura, K Hosoda, S Masui, K Nakao, J Miyazaki Ji and H Niwa. (2002). Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev 16:784-789. (Pubitemid 34280102)
36. Morrisey EE, Z Tang, K Sigrist, MM Lu, F Jiang, HS Ip and MS Parmacek. (1998). GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev 12:3579-3590. (Pubitemid 28553248)
37. Cai KQ, CD Capo-Chichi, ME Rula, DH Yang and XX Xu. (2008). Dynamic GATA6 expression in primitive endoderm formation and maturation in early mouse embryogenesis. Dev Dyn 237:2820-2829.
38. Costa RH, DR Grayson and JE Darnell, Jr. (1989). Multiple hepatocyte-enriched nuclear factors function in the regulation of transthyretin and alpha 1-antitrypsin genes. Mol Cell Biol 9:1415-1425. (Pubitemid 19095181)
39. Ang SL, A Wierda, D Wong, KA Stevens, S Cascio, J Rossant and KS Zaret. (1993). The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119:1301-1315. (Pubitemid 23358595)
40. Ang SL and J Rossant. (1994). HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78:561-574.
41. Monaghan AP, KH Kaestner, E Grau and G Schutz. (1993). Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm. Development 119:567-578. (Pubitemid 23337404)
42. Dufort D, L Schwartz, K Harpal and J Rossant. (1998). The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 125:3015-3025. (Pubitemid 28434402)
43. Enders AC and S Schlafke. (1978). Comparative aspects of blastocyst-endometrial interactions at implantation. Ciba Found Symp:3-32.
44. Thomas P and R Beddington. (1996). Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr Biol 6:1487-1496. (Pubitemid 27012247)
45. Weinstein DC, A Ruiz i Altaba, WS Chen, P Hoodless, VR Prezioso, TM Jessell and JE Darnell, Jr. (1994). The wingedhelix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78:575-588. (Pubitemid 24268581)
46. Shimosato D, M Shiki and H Niwa. (2007). Extra-embryonic endoderm cells derived from ES cells induced by GATA factors acquire the character of XEN cells. BMC Dev Biol 7:80.
47. Reichel RR, S Budhiraja and A Jacob. (1994). Delayed activation of HNF-3 beta upon retinoic acid-induced teratocarcinoma cell differentiation. Exp Cell Res 214:634-641.
48. Jacob A, S Budhiraja, X Qian, D Clevidence, RH Costa and RR Reichel. (1994). Retinoic acid-mediated activation of HNF-3 alpha during EC stem cell differentiation. Nucleic Acids Res 22:2126-2133. (Pubitemid 24192915)
49. Futaki S, Y Hayashi, T Emoto, CN Weber and K Sekiguchi. (2004). Sox7 plays crucial roles in parietal endoderm differentiation in F9 embryonal carcinoma cells through regulating Gata-4 and Gata-6 expression. Mol Cell Biol 24:10492-10503. (Pubitemid 39507885)
50. Kemler R, P Brulet, MT Schnebelen, J Gaillard and F Jacob. (1981). Reactivity of monoclonal antibodies against intermediate filament proteins during embryonic development. J Embryol Exp Morphol 64:45-60. (Pubitemid 11039709)
51. Biechele TL and RT Moon. (2008). Assaying beta-catenin/ TCF transcription with beta-catenin/TCF transcriptionbased reporter constructs. Methods Mol Biol 468:99-110.
52. Nakamura T, A Fox-Robichaud, R Kikkawa, A Kashiwagi, H Kojima, M Fujimiya and NC Wong. (1999). Transcription factors and age-related decline in apolipoprotein A-I expression. J Lipid Res 40:1709-1718. (Pubitemid 29418713)
53. Yokoyama H, H Harigae, S Takahashi, K Furuyama, M Kaku, M Yamamoto and T Sasaki. (2003). Regulation of YB-1 gene expression by GATA transcription factors. Biochem Biophys Res Commun 303:140-145. (Pubitemid 36338219)
54. Denson LA, MH McClure, CW Bogue, SJ Karpen and HC Jacobs. (2000). HNF3beta and GATA-4 transactivate the liver-enriched homeobox gene, Hex. Gene 246:311-320. (Pubitemid 30190185)
55. Soudais C, M Bielinska, M Heikinheimo, CA MacArthur, N Narita, JE Saffitz, MC Simon, JM Leiden and DB Wilson. (1995). Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121: 3877-3888.
56. Sepulveda JL, N Belaguli, V Nigam, CY Chen, M Nemer and RJ Schwartz. (1998). GATA-4 and Nkx-2. coactivate Nkx-2 DNA binding targets: role for regulating early cardiac gene expression. Mol Cell Biol 18:3405-3415. (Pubitemid 28240513)
57. Weiler-Guettler H, K Yu, G Soff, LJ Gudas and RD Rosenberg. (1992). Thrombomodulin gene regulation by cAMP and retinoic acid in F9 embryonal carcinoma cells. Proc Natl Acad Sci U S A 89:2155-2159.
58. Artus J, A Piliszek and AK Hadjantonakis. (2011). The primitive endoderm lineage of the mouse blastocyst: sequential transcription factor activation and regulation of differentiation by Sox17. Dev Biol 350:393-404.
59. Vidigal JA, M Morkel, L Wittler, A Brouwer-Lehmitz, P Grote, K Macura and BG Herrmann. (2010). An inducible RNA interference system for the functional dissection of mouse embryogenesis. Nucleic Acids Res 38:e122.
60. Wang Y, JL Smedberg, KQ Cai, DC Capo-Chichi and XX Xu. (2011). Ectopic expression of GATA6 bypasses requirement for Grb2 in primitive endoderm formation. Dev Dyn 240: 566-576.
61. Plusa B, A Piliszek, S Frankenberg, J Artus and AK Hadjantonakis. (2008). Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135:3081-3091.
62. Brown K, S Legros, J Artus, MX Doss, R Khanin, AK Hadjantonakis and A Foley. (2010). A comparative analysis of extra-embryonic endoderm cell lines. PLoS One 5:e12016.
63. Tamplin OJ, D Kinzel, BJ Cox, CE Bell, J Rossant and H Lickert. (2008). Microarray analysis of Foxa2 mutant mouse embryos reveals novel gene expression and inductive roles for the gastrula organizer and its derivatives. BMC Genomics 9:511.
64. McKnight KD, J Hou and PA Hoodless. (2010). Foxh1 and Foxa2 are not required for formation of the midgut and hindgut definitive endoderm. Dev Biol 337:471-481.
65. Lavery DL, J Martin, YD Turnbull and S Hoppler. (2008). Wnt6 signaling regulates heart muscle development during organogenesis. Dev Biol 323:177-188.
66. Prieve MG and ML Waterman. (1999). Nuclear localization and formation of beta-catenin-lymphoid enhancer factor 1 complexes are not sufficient for activation of gene expression. Mol Cell Biol 19:4503-4515. (Pubitemid 29242023)
67. Capo-Chichi CD, JL Smedberg, M Rula, E Nicolas, AT Yeung, RF Adamo, A Frolov, AK Godwin and XX Xu. (2010). Alteration of differentiation potentials by modulating GATA transcription factors in murine embryonic stem cells. Stem Cells Int 2010:602068.
68. Morrisey EE, S Musco, MY Chen, MM Lu, JM Leiden and MS Parmacek. (2000). The gene encoding the mitogenresponsive phosphoprotein Dab2 is differentially regulated by GATA-6 and GATA-4 in the visceral endoderm. J Biol Chem 275:19949-19954. (Pubitemid 30441601)
69. Wang R, J Liang, HM Yu, H Liang, YJ Shi and HT Yang. (2008). Retinoic acid maintains self-renewal of murine embryonic stem cells via a feedback mechanism. Differentiation 76:931-945.
70. Wang QT, K Piotrowska, MA Ciemerych, L Milenkovic, MP Scott, RW Davis and M Zernicka-Goetz. (2004). A genomewide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6:133-144. (Pubitemid 38089211)
71. Lloyd S, TP Fleming and JE Collins. (2003). Expression of Wnt genes during mouse preimplantation development. Gene Expr Patterns 3:309-312. (Pubitemid 36675997)
72. Galceran J, SC Hsu and R Grosschedl. (2001). Rescue of a Wnt mutation by an activated form of LEF-1: regulation of maintenance but not initiation of Brachyury expression. Proc Natl Acad Sci U S A 98:8668-8673. (Pubitemid 32678085)
73. Mohamed OA, D Dufort and HJ Clarke. (2004). Expression and estradiol regulation of Wnt genes in the mouse blastocyst identify a candidate pathway for embryo-maternal signaling at implantation. Biol Reprod 71:417-424. (Pubitemid 38970514)
74. Wang J and A Wynshaw-Boris. (2004). The canonical Wnt pathway in early mammalian embryogenesis and stem cell maintenance/differentiation. Curr Opin Genet Dev 14:533-539. (Pubitemid 39360301)
75. Monkley SJ, SJ Delaney, DJ Pennisi, JH Christiansen and BJ Wainwright. (1996). Targeted disruption of the Wnt2 gene results in placentation defects. Development 122:3343-3353. (Pubitemid 26395977)
76. Parr BA and AP McMahon. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374:350-353.
77. Inoue A, A Nagafuchi and A Kikuchi. (2009). Retinoic acid induces discrete Wnt-signaling-dependent differentiation in F9 cells. Biochem Biophys Res Commun 390:564-569.
78. Potok MA, KB Cha, A Hunt, ML Brinkmeier, M Leitges, A Kispert and SA Camper. (2008). WNT signaling affects gene expression in the ventral diencephalon and pituitary gland growth. Dev Dyn 237:1006-1020. (Pubitemid 351542297)
79. Weidenfeld J, W Shu, L Zhang, SE Millar and EE Morrisey. (2002). The WNT7b promoter is regulated by TTF-1, GATA6, and Foxa2 in lung epithelium. J Biol Chem 277:21061-21070. (Pubitemid 34967417)
80. Wang Z, W Shu, MM Lu and EE Morrisey. (2005). Wnt7b activates canonical signaling in epithelial and vascular smooth muscle cells through interactions with Fzd1, Fzd10, and LRP5. Mol Cell Biol 25:5022-5030. (Pubitemid 40781102)