Modulation of Tcf3 repressor complex composition regulates cdx4 expression in zebrafish

EMBO Journal

Volumn 30, Issue 14, 2011, Pages 2894-2907

  Ro, Hyunju ^a   Dawid, Igor B ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Caudal body domain; Cdx4; E4f1; Tcf3; Wnt signalling

Indexed keywords

COREPRESSOR PROTEIN; DNA; HISTONE DEACETYLASE 1; PEPTIDES AND PROTEINS; PROTEIN CDX4; PROTEIN E4F1; SCAFFOLD PROTEIN; TRANSCRIPTION FACTOR 7 LIKE 1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE REPRESSION; MAMMAL CELL; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; TAIL; ZEBRA FISH;

ANIMALS; BLOTTING, WESTERN; BODY PATTERNING; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEACETYLASE 1; HOMEODOMAIN PROTEINS; IMMUNOPRECIPITATION; LUCIFERASES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; UBIQUITIN-PROTEIN LIGASES; WNT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; MAMMALIA;

EID: 79960645983     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.184     Document Type: Article

References (74)

1. Abu-Remaileh M, Gerson A, Farago M, Nathan G, Alkalay I, Zins Rousso S, Gur M, Fainsod A, Bergman Y (2010) Oct-3/4 regulates stem cell identity and cell fate decisions by modulating Wnt/b-catenin signalling. EMBO J 29: 3236-3248
2. Bai X, Kim J, Yang Z, Jurynec MJ, Akie TE, Lee J, LeBlanc J, Sessa A, Jiang H, DiBiase A, Zhou Y, Grunwald DJ, Lin S, Cantor AB, Orkin SH, Zon LI (2010) TIF1g controls erythroid cell fate by regulating transcription elongation. Cell 142: 133-143
3. Bansal D, Scholl C, Fröhling S, McDowell E, Lee BH, Döhner K, Ernst P, Davidson AJ, Daley GQ, Zon LI, Gilliland DG, Huntly BJ (2006) Cdx4 dysregulates Hox gene expression and generates acute myeloid leukemia alone and in cooperation with Meis1a in a murine model. Proc Natl Acad Sci USA 103: 16924-16929 (Pubitemid 44737354)
4. Billin AN, Thirlwell H, Ayer DE (2000) b-catenin-histone deacety-lase interactions regulate the transition of LEF1 from a transcrip-tional repressor to an activator. Mol Cell Biol 20: 6882-6890
5. Bonkowsky JL, Wang X, Fujimoto E, Lee JE, Chien CB, Dorsky RI (2008) Domain-specific regulation of foxP2 CNS expression by lef1. BMC Dev Biol 8: 103
6. Brannon M, Gomperts M, Sumoy L, Moon RT, Kimelman D (1997) A b-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev 11 : 2359-2370 (Pubitemid 27408533)
7. Brantjes H, Roose J, van De Wetering M, Clevers H (2001) All Tcf HMG box transcription factors interact with Groucho-related corepressors. Nucleic Acids Res 29: 1410-1419 (Pubitemid 32288486)
8. Cavallo RA, Cox RT, Moline MM, Roose J, Polevoy GA, Clevers H, Peifer M, Bejsovec A (1998) Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395: 604-608 (Pubitemid 28475714)
9. Chagraoui J, Niessen SL, Lessard J, Girard S, Coulombe P, Sauvageau M, Meloche S, Sauvageau G (2006) E4f1: a novel candidate factor for mediating BMI1 function in primitive hematopoietic cells. Genes Dev 20: 2110-2120 (Pubitemid 44157461)
10. Chen YH, Lu YF, Ko TY, Tsai MY, Lin CY, Lin CC, Hwang SP (2009) Zebrafish cdx1b regulates differentiation of various intestinal cell lineages. Dev Dyn 238: 1021-1032
11. Cheng PY, Lin CC, Wu CS, Lu YF, Lin CY, Chung CC, Chu CY, Huang CJ, Tsai CY, Korzh S, Wu JL, Hwang SP (2008) Zebrafish cdx1b regulates expression of downstream factors of Nodal signaling during early endoderm formation. Development 135: 941-952 (Pubitemid 351524148)
12. Colombo R, Draetta GF, Chiocca S (2003) Modulation of p120E4f1 transcriptional activity by the Gam1 adenoviral early protein. Oncogene 22: 2541-2547 (Pubitemid 36605601)
13. Davidson AJ, Ernst P, Wang Y, Dekens MP, Kingsley PD, Palis J, Korsmeyer SJ, Daley GQ, Zon LI (2003) cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature 425: 300-306 (Pubitemid 37158406)
14. Davidson AJ, Zon LI (2004) The 'definitive' (and 'primitive') guide to zebrafish hematopoiesis. Oncogene 23: 7233-7246 (Pubitemid 39382157)
15. Dorsky RI, Itoh M, Moon RT, Chitnis A (2003) Two tcf3 genes cooperate to pattern the zebrafish brain. Development 130: 1937-1947 (Pubitemid 36575919)
16. Dorsky RI, Snyder A, Cretekos CJ, Grunwald DJ, Geisler R, Haffter P, Moon RT, Raible DW (1999) Maternal and embryonic expression of zebrafish lef1. Mech Dev 86: 147-150 (Pubitemid 29371751)
17. Erter CE, Wilm TP, Basler N, Wright CV, Solnica-Krezel L (2001) Wnt8 is required in lateral mesendodermal precursors for neural posteriorization in vivo. Development 128: 3571-3583 (Pubitemid 32962724)
18. Faas L, Isaacs HV (2009) Overlapping functions of Cdx1, Cdx2, and Cdx4 in the development of the amphibian Xenopus tropicalis. Dev Dyn 238: 835-852
19. Fajas L, Paul C, Vié A, Estrach S, Medema R, Blanchard JM, Sardet C, Vignais ML (2001) Cyclin A is a mediator of p120E4F-dependent cell cycle arrest in G1. Mol Cell Biol 21: 2956-2966 (Pubitemid 32244937)
20. Fernandes ER, Rooney RJ (1997) The adenovirus E1A-regulated transcription factor E4F is generated from the human homolog of nuclear factor phiAP3. Mol Cell Biol 17: 1890-1903 (Pubitemid 27133274)
21. Flores MV, Hall CJ, Davidson AJ, Singh PP, Mahagaonkar AA, Zon LI, Crosier KE, Crosier PS (2008) Intestinal differentiation in zebrafish requires Cdx1b, a functional equivalent of mammalian Cdx2. Gastroenterology 135: 1665-1675
22. Fredieu JR, Cui Y, Maier D, Danilchik MV, Christian JL (1997) Xwnt-8 and lithium can act upon either dorsal mesodermal or neurectodermal cells to cause a loss of forebrain in Xenopus embryos. Dev Biol 186: 100-114 (Pubitemid 27314376)
23. Galceran J, Fariñas I, Depew MJ, Clevers H, Grosschedl R (1999) Wnt3a-/-like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev 13: 709-717 (Pubitemid 29155977)
24. Gao N, Kaestner KH (2010) Cdx2 regulates endo-lysosomal function and epithelial cell polarity. Genes Dev 24: 1295-1305
25. Gat U, DasGupta R, Degenstein L, Fuchs E (1998) De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated b-catenin in skin. Cell 95: 605-614 (Pubitemid 28544122)
26. Gribble SL, Kim HS, Bonner J, Wang Xu, Dorsky RI (2009) Tcf3 inhibits spinal cord neurogenesis by regulating sox4a expression. Development 136: 781-789
27. Hikasa H, Ezan J, Itoh K, Li X, Klymkowsky MW, Sokol SY (2010) Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev Cell 19: 521-532
28. Hofmayer S, Madisch I, Darr S, Rehren F, Heim A (2009) Unique sequence features of the human adenovirus 31 complete genomic sequence are conserved in clinical isolates. BMC Genomics 10: 557
29. Honda T, Yamamoto H, Ishii A, Inui M (2010) PDZRN3 negatively regulates BMP-2-induced osteoblast differentiation through inhibition of Wnt signaling. Mol Biol Cell 21 : 3269-3277
30. Hovanes K, Li TW, Munguia JE, Truong T, Milovanovic T, Lawrence Marsh J, Holcombe RF, Waterman ML (2001) b-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat Genet 28: 53-57 (Pubitemid 32405817)
31. Hurlstone A, Clevers H (2002) T-cell factors: turn-ons and turn-offs. EMBO J 21: 2303-2311 (Pubitemid 34546703)
32. Iimura T, Denans N, Pourquié O (2009) Establishment of Hox vertebral identities in the embryonic spine precursors. Curr Top Dev Biol 88: 201-234
33. Isaacs HV, Pownall ME, Slack JM (1998) Regulation of Hox gene expression and posterior development by the Xenopus caudal homologue Xcad3. EMBO J 17: 3413-3427 (Pubitemid 28279514)
34. Jiang J, Chan YS, Loh YH, Cai J, Tong GQ, Lim CA, Robson P, Zhong S, Ng HH (2008) A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol 10 : 353-360 (Pubitemid 351331023)
35. Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7: 133-144 (Pubitemid 39172695)
36. Kim CH, Oda T, Itoh M, Jiang D, Artinger KB, Chandrasekharappa SC, Driever W, Chitnis AB (2000) Repressor activity of headless/Tcf3 is essential for vertebrate head formation. Nature 407: 913-916
37. Kim MJ, Kang KH, Kim CH, Choi SY (2008) Real-time imaging of mitochondria in transgenic zebrafish expressing mitochondrially targeting GFP. Biotechniques 45: 331-334
38. Lacroix M, Caramel J, Goguet-Rubio P, Linares LK, Estrach S, Hatchi E, Rodier G, Lledo G, de Bettignies C, Thépot A, Deraison C, Chébli K, Hovnanian A, Hainaut P, Dubus P, Sardet C, Le Cam L (2010) Transcription factor E4F1 is essential for epidermal stem cell maintenance and skin homeostasis. Proc Natl Acad Sci USA 107 : 21076-21081
39. Le Cam L, Lacroix M, Ciemerych MA, Sardet C, Sicinski P (2004) The E4F protein is required for mitotic progression during embryonic cell cycles. Mol Cell Biol 24: 6467-6475 (Pubitemid 38891145)
40. Le Cam L, Linares LK, Paul C, Julien E, Lacroix M, Hatchi E, Triboulet R, Bossis G, Shmueli A, Rodriguez MS, Coux O, Sardet C (2006) E4f1 is an atypical ubiquitin ligase that modulates p53 effector functions independently of degradation. Cell 127: 775-788 (Pubitemid 44716249)
41. Lee JE, Wu SF, Goering LM, Dorsky RI (2006) Canonical Wnt signaling through Lef1 is required for hypothalamic neuro-genesis. Development 133: 4451-4461 (Pubitemid 46017820)
42. Lekven AC, Thorpe CJ, Waxman JS, Moon RT (2001) Zebrafish wnt8 encodes two Wnt8 proteins on a bicistronic transcript and is required for mesoderm and neurectoderm patterning. Dev Cell 1: 103-114 (Pubitemid 33586073)
43. Lengerke C, Schmitt S, Bowman TV, Jang IH, Maouche-Chretien L, McKinney-Freeman S, Davidson AJ, Hammerschmidt M, Rentzsch F, Green JB, Zon LI, Daley GQ (2008) BMP and Wnt specify hematopoietic fate by activation of the Cdx-Hox pathway. Cell Stem Cell 2: 72-82
44. Li Z, Nie F, Wang S, Li L (2011) Histone H4 Lys 20 monomethylation by histone methylase SET8 mediates Wnt target gene activation. Proc Natl Acad Sci USA 108: 3116-3123
45. MacDonald BT, Tamai K, He X (2009) Wnt/b-catenin signaling: components, mechanisms, and diseases. Dev Cell 17: 9-26
46. Mallo M, Vinagre T, Carapuço M (2009) The road to the vertebral formula. Int J Dev Biol 53: 1469-1481
47. Merrill BJ, Pasolli HA, Polak L, Rendl M, Garća-Garća MJ, Anderson KV, Fuchs E (2004) Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 131: 263-274 (Pubitemid 38181367)
48. Nagayoshi S, Hayashi E, Abe G, Osato N, Asakawa K, Urasaki A, Horikawa K, Ikeo K, Takeda H, Kawakami K (2008) Insertional mutagenesis by the Tol2 transposon-mediated enhancer trap approach generated mutations in two developmental genes: tcf7 and synembryn-like. Development 135: 159-169 (Pubitemid 351201489)
49. Nelson JD, Denisenko O, Bomsztyk K (2006) Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat Protoc 1: 179-185
50. Nguyen H, Merrill BJ, Polak L, Nikolova M, Rendl M, Shaver TM, Pasolli HA, Fuchs E (2009) Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat Genet 41: 1068-1075
51. Nie J, McGill MA, Dermer M, Dho SE, Wolting CD, McGlade CJ (2002) LNX functions as a RING type E3 ubiquitin ligase that targets the cell fate determinant Numb for ubiquitin-dependent degradation. EMBO J 21 : 93-102 (Pubitemid 34087078)
52. Nordström U, Maier E, Jessell TM, Edlund T (2006) An early role for WNT signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity. PLoS Biol 4: e252
53. Pilon N, Oh K, Sylvestre JR, Bouchard N, Savory J, Lohnes D (2006) Cdx4 is a direct target of the canonical Wnt pathway. Dev Biol 289: 55-63 (Pubitemid 41804088)
54. Pilon N, Oh K, Sylvestre JR, Savory JGA, Lohnes D (2007) Wnt signalling is a key mediator of cdx1 expression in vivo. Development 134: 2315-2323 (Pubitemid 47010020)
55. Riedt T, Ebinger M, Salih HR, Tomiuk J, Handgretinger R, Kanz L, Grünebach F, Lengerke C (2009) Aberrant expression of the homeobox gene CDX2 in pediatric acute lymphoblastic leukemia. Blood 113: 4049-4051
56. Ro H, Dawid IB (2009) Organizer restriction through modulation of Bozozok stability by the E3 ubiquitin ligase Lnx-like. Nat Cell Biol 11 : 1121-1127
57. Ro H, Dawid IB (2010) Lnx-2b restricts gsc expression to the dorsal mesoderm by limiting Nodal and Bozozok activity. Biochem Biophys Res Commun 402: 626-630
58. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA, Ekker SC (2007) p53 activation by knockdown technologies. PLoS Genet 3: e7
59. Roël G, Hamilton FS, Gent Y, Bain AA, Destrée O, Hoppler S (2002) Lef-1 and Tcf-3 transcription factors mediate tissue-specific Wnt signaling during Xenopus development. Curr Biol 12: 1941-1945 (Pubitemid 35426708)
60. Ruzov A, Hackett JA, Prokhortchouk A, Reddington JP, Madej MJ, Dunican DS, Prokhortchouk E, Pennings S, Meehan RR (2009) The interaction of xKaiso with xTcf3: a revised model for integra-tion of epigenetic and Wnt signaling pathways. Development 136: 723-727
61. Scholl C, Bansal D, Döhner K, Eiwen K, Huntly BJ, Lee BH, Rücker FG, Schlenk RF, Bullinger L, Döhner H, Gilliland DG, Fröhling S (2007) The homeobox gene CDX2 is aberrantly expressed in most cases of acute myeloid leukemia and promotes leukemogenesis. J Clin Invest 117: 1037-1048 (Pubitemid 46556760)
62. Shimizu T, Bae YK, Muraoka O, Hibi M (2005) Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev Biol 279: 125-141 (Pubitemid 40222174)
63. Snider L, Thirlwell H, Miller JR, Moon RT, Groudine M, Tapscott SJ (2001) Inhibition of Tcf3 binding by I-mfa domain proteins. Mol Cell Biol 21 : 1866-1873 (Pubitemid 32156406)
64. Thoene S, Rawat VP, Heilmeier B, Hoster E, Metzeler KH, Herold T, Hiddemann W, Gökbuget N, Hoelzer D, Bohlander SK, Feuring-Buske M, Buske C (2009) The homeobox gene CDX2 is aberrantly expressed and associated with an inferior prognosis in patients with acute lymphoblastic leukemia. Leukemia 23: 649-655
65. Thorpe CJ, Weidinger G, Moon RT (2005) Wnt/beta-catenin regulation of the Sp1-related transcription factor sp5l promotes tail development in zebrafish. Development 132: 1763-1772 (Pubitemid 40691767)
66. Van den Akker E, Forlani S, Chawengsaksophak K, de Graaff W, Beck F, Meyer BI, Deschamps J (2002) Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 129: 2181-2193 (Pubitemid 34874231)
67. Veien ES, Grierson MJ, Saund RS, Dorsky RI (2005) Expression pattern of zebrafish tcf7 suggests unexplored domains of Wnt/b-catenin activity. Dev Dyn 233: 233-239 (Pubitemid 40548042)
68. Wang Y, Yabuuchi A, McKinney-Freeman S, Ducharme DM, Ray MK, Chawengsaksophak K, Archer TK, Daley GQ (2008) Cdx gene deficiency compromises embryonic hematopoiesis in the mouse. Proc Natl Acad Sci USA 105 : 7756-7761 (Pubitemid 351872711)
69. Yamaguchi M, Tonou-Fujimori N, Komori A, Maeda R, Nojima Y, Li H, Okamoto H, Masai I (2005) Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and notch signaling pathways. Development 132: 3027-3043 (Pubitemid 41086737)
70. Yan D, Lin X (2009) Shaping morphogen gradients by proteogly-cans. Cold Spring Harb Perspect Biol 1: a002493
71. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the b-catenin-TCF interaction. Nat Neurosci 12: 829-838
72. Young RM, Reyes AE, Allende ML (2002) Expression and splice variant analysis of the zebrafish tcf4 transcription factor. Mech Dev 117: 269-273 (Pubitemid 36158733)
73. Young T, Deschamps J (2009) Hox, Cdx, and anteroposterior patterning in the mouse embryo. Curr Top Dev Biol 88: 235-255
74. Young T, Rowland JE, van de Ven C, Bialecka M, Novoa A, Carapuco M, van Nes J, de Graaff W, Duluc I, Freund JN, Beck F, Mallo M, Deschamps J (2009) Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev Cell 17: 516-526