Function of Wnt/β-catenin in counteracting Tcf3 repression through the Tcf3-β-catenin interaction

Development (Cambridge)

Volumn 139, Issue 12, 2012, Pages 2118-2129

  Wu, Chun I ^a   Hoffman, Jackson A ^a   Shy, Brian R ^a   Ford, Erin M ^b   Fuchs, Elaine ^c   Nguyen, Hoang ^b   Merrill, Bradley J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Beta catenin; Embryonic stem cell; Mouse embryogenesis; Tcf3; Wnt signaling

Indexed keywords

BETA CATENIN; LYMPHOID ENHANCER FACTOR 1; MESSENGER RNA; TRANSCRIPTION FACTOR 7 LIKE 1; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EYELID CLOSURE; FEMALE; GASTRULATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; IN VIVO STUDY; LIMB DEVELOPMENT; MALE; MOUSE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BETA CATENIN; BODY PATTERNING; EMBRYONIC STEM CELLS; EXTREMITIES; EYELIDS; GASTRULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCK-IN TECHNIQUES; HEDGEHOG PROTEINS; LIMB BUDS; LYMPHOID ENHANCER-BINDING FACTOR 1; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; PROTEIN BINDING; REPRESSOR PROTEINS; SURVIVAL ANALYSIS; WNT SIGNALING PATHWAY;

ANURA; MUS;

EID: 84861362271     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.076067     Document Type: Article

References (72)

1. Aberle, H., Bauer, A., Stappert, J., Kispert, A. and Kemler, R. (1997). Betacatenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797-3804.
2. Arnold, S. J., Stappert, J., Bauer, A., Kispert, A., Herrmann, B. G. and Kemler, R. (2000). Brachyury is a target gene of the Wnt/beta-catenin signaling pathway. Mech. Dev. 91, 249-258.
3. Atcha, F. A., Syed, A., Wu, B., Hoverter, N. P., Yokoyama, N. N., Ting, J. H., Munguia, J. E., Mangalam, H. J., Marsh, J. L. and Waterman, M. L. (2007). A unique DNA binding domain converts T-cell factors into strong Wnt effectors. Mol. Cell. Biol. 27, 8352-8363.
4. Barker, N., Hurlstone, A., Musisi, H., Miles, A., Bienz, M. and Clevers, H. (2001). The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J. 20, 4935-4943.
5. Behrens, J., von Kries, J. P., Kuhl, M., Bruhn, L., Wedlich, D., Grosschedl, R. and Birchmeier, W. (1996). Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382, 638-642.
6. Behrens, J., Jerchow, B. A., Wurtele, M., Grimm, J., Asbrand, C., Wirtz, R., Kuhl, M., Wedlich, D. and Birchmeier, W. (1998). Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280, 596-599.
7. Ben-Porath, I., Thomson, M. W., Carey, V. J., Ge, R., Bell, G. W., Regev, A. and Weinberg, R. A. (2008). An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 40, 499-507.
8. Brannon, M., Gomperts, M., Sumoy, L., Moon, R. T. and Kimelman, D. (1997). A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev. 11, 2359-2370.
9. Brantjes, H., Roose, J., van De Wetering, M. and Clevers, H. (2001). All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res. 29, 1410-1419.
10. DasGupta, R. and Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568.
11. Dorsky, R. I., Itoh, M., Moon, R. T. and Chitnis, A. (2003). Two tcf3 genes cooperate to pattern the zebrafish brain. Development 130, 1937-1947.
12. Filali, M., Cheng, N., Abbott, D., Leontiev, V. and Engelhardt, J. F. (2002). Wnt-3A/beta-catenin signaling induces transcription from the LEF-1 promoter. J. Biol. Chem. 277, 33398-33410.
13. Findlater, G. S., McDougall, R. D. and Kaufman, M. H. (1993). Eyelid development, fusion and subsequent reopening in the mouse. J. Anat. 183, 121-129.
14. -/- mice. Genes Dev. 13, 709-717.
15. Galceran, J., Hsu, S. C. and Grosschedl, R. (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. USA 98, 8668-8673.
16. Graham, T. A., Weaver, C., Mao, F., Kimelman, D. and Xu, W. (2000). Crystal structure of a beta-catenin/Tcf complex. Cell 103, 885-896.
17. Graham, T. A., Ferkey, D. M., Mao, F., Kimelman, D. and Xu, W. (2001). Tcf4 can specifically recognize beta-catenin using alternative conformations. Nat. Struct. Biol. 8, 1048-1052.
18. Gray, J. D., Nakouzi, G., Slowinska-Castaldo, B., Dazard, J. E., Rao, J. S., Nadeau, J. H. and Ross, M. E. (2010). Functional interactions between the LRP6 WNT co-receptor and folate supplementation. Hum. Mol. Genet. 19, 4560-4572.
19. Hecht, A. and Stemmler, M. P. (2003). Identification of a promoter-specific transcriptional activation domain at the C terminus of the Wnt effector protein T-cell factor 4. J. Biol. Chem. 278, 3776-3785.
20. Hecht, A., Vleminckx, K., Stemmler, M. P., van Roy, F. and Kemler, R. (2000). The p300/CBP acetyltransferases function as transcriptional coactivators of betacatenin in vertebrates. EMBO J. 19, 1839-1850.
21. Houston, D. W., Kofron, M., Resnik, E., Langland, R., Destree, O., Wylie, C. and Heasman, J. (2002). Repression of organizer genes in dorsal and ventral Xenopus cells mediated by maternal XTcf3. Development 129, 4015-4025.
22. Hovanes, K., Li, T. W., Munguia, J. E., Truong, T., Milovanovic, T., Lawrence Marsh, J., Holcombe, R. F. and Waterman, M. L. (2001). Beta-cateninsensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat. Genet. 28, 53-57.
23. Huelsken, J., Vogel, R., Brinkmann, V., Erdmann, B., Birchmeier, C. and Birchmeier, W. (2000). Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148, 567-578.
24. Ikeda, S., Kishida, S., Yamamoto, H., Murai, H., Koyama, S. and 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.
25. Ishikawa, T. O., Tamai, Y., Li, Q., Oshima, M. and Taketo, M. M. (2003). Requirement for tumor suppressor Apc in the morphogenesis of anterior and ventral mouse embryo. Dev. Biol. 253, 230-246.
26. Ivanova, N. B., Dimos, J. T., Schaniel, C., Hackney, J. A., Moore, K. A. and Lemischka, I. R. (2002). A stem cell molecular signature. Science 298, 601-604.
27. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N. and Costantini, F. (2002). Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183.
28. Kelly, K. F., Ng, D. Y., Jayakumaran, G., Wood, G. A., Koide, H. and Doble, B. W. (2011). beta-catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 8, 214-227.
29. Kelly, O. G., Pinson, K. I. and Skarnes, W. C. (2004). The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131, 2803-2815.
30. Kemler, R., Hierholzer, A., Kanzler, B., Kuppig, S., Hansen, K., Taketo, M. M., de Vries, W. N., Knowles, B. B. and Solter, D. (2004). Stabilization of betacatenin in the mouse zygote leads to premature epithelial-mesenchymal transition in the epiblast. Development 131, 5817-5824.
31. Kengaku, M., Capdevila, J., Rodriguez-Esteban, C., De La Pena, J., Johnson, R. L., Izpisua Belmonte, J. C. and Tabin, C. J. (1998). Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280, 1274-1277.
32. Khokha, M. K., Hsu, D., Brunet, L. J., Dionne, M. S. and Harland, R. M. (2003). Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat. Genet. 34, 303-307.
33. Kim, C. H., Oda, T., Itoh, M., Jiang, D., Artinger, K. B., Chandrasekharappa, S. C., Driever, W. and Chitnis, A. B. (2000). Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature 407, 913-916.
34. Knop, E., Korb, D. R., Blackie, C. A. and Knop, N. (2010). The lid margin is an underestimated structure for preservation of ocular surface health and development of dry eye disease. Dev. Ophthalmol. 45, 108-122.
35. Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., Murone, M., Zullig, S. and Basler, K. (2002). Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell 109, 47-60.
36. Laufer, E., Nelson, C. E., Johnson, R. L., Morgan, B. A. and Tabin, C. (1994). Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79, 993-1003.
37. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X. and He, X. (2002). Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847.
38. Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R. and Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22, 361-365.
39. Liu, S., Li, J., Tan, D. T. and Beuerman, R. W. (2007). The eyelid margin: a transitional zone for 2 epithelial phenotypes. Arch. Ophthalmol. 125, 523-532.
40. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
41. Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M. and Piccolo, S. (2003). Mapping Wnt/betacatenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304.
42. Merrill, B. J., Gat, U., DasGupta, R. and Fuchs, E. (2001). Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 15, 1688-1705.
43. Merrill, B. J., Pasolli, H. A., Polak, L., Rendl, M., Garcia-Garcia, M. J., Anderson, K. V. and Fuchs, E. (2004). Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 131, 263-274.
44. Molenaar, M., van de Wetering, M., Oosterwegel, M., Peterson-Maduro, J., Godsave, S., Korinek, V., Roose, J., Destree, O. and Clevers, H. (1996). XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86, 391-399.
45. Moon, R. T., Bowerman, B., Boutros, M. and Perrimon, N. (2002). The promise and perils of Wnt signaling through beta-catenin. Science 296, 1644-1646.
46. Nguyen, H., Rendl, M. and Fuchs, E. (2006). Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 127, 171-183.
47. Niswander, L., Jeffrey, S., Martin, G. R. and Tickle, C. (1994). A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371, 609-612.
48. Parr, B. A. and McMahon, A. P. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350-353.
49. Pereira, L., Yi, F. and Merrill, B. J. (2006). Repression of nanog gene transcription by tcf3 limits embryonic stem cell self-renewal. Mol. Cell. Biol. 26, 7479-7491.
50. Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J. and Skarnes, W. C. (2000). An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407, 535-538.
51. Popperl, H., Schmidt, C., Wilson, V., Hume, C. R., Dodd, J., Krumlauf, R. and Beddington, R. S. (1997). Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm. Development 124, 2997-3005.
52. Rendl, M., Lewis, L. and Fuchs, E. (2005). Molecular dissection of esenchymalepithelial interactions in the hair follicle. PLoS Biol. 3, e331.
53. Riau, A. K., Barathi, V. A. and Beuerman, R. W. (2008). Mucocutaneous junction of eyelid and lip: a study of the transition zone using epithelial cell markers. Curr. Eye Res. 33, 912-922.
54. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
55. Roose, J., Huls, G., van Beest, M., Moerer, P., van der Horn, K., Goldschmeding, R., Logtenberg, T. and Clevers, H. (1999). Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 285, 1923-1926.
56. Sun, Y., Kolligs, F. T., Hottiger, M. O., Mosavin, R., Fearon, E. R. and Nabel, G. J. (2000). Regulation of beta -catenin transformation by the p300 transcriptional coactivator. Proc. Natl. Acad. Sci. USA 97, 12613-12618.
57. Takemaru, K. I. and Moon, R. T. (2000). The transcriptional coactivator CBP interacts with beta-catenin to activate gene expression. J. Cell Biol. 149, 249-254.
58. Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, F., Saint-Jeannet, J. P. and He, X. (2000). LDL-receptor-related proteins in Wnt signal transduction. Nature 407, 530-535.
59. Tao, H., Shimizu, M., Kusumoto, R., Ono, K., Noji, S. and Ohuchi, H. (2005). A dual role of FGF10 in proliferation and coordinated migration of epithelial leading edge cells during mouse eyelid development. Development 132, 3217-3230.
60. van Beest, M., Dooijes, D., van De Wetering, M., Kjaerulff, S., Bonvin, A., Nielsen, O. and Clevers, H. (2000). Sequence-specific high mobility group box factors recognize 10-12-base pair minor groove motifs. J. Biol. Chem. 275, 27266-27273.
61. van de Wetering, M. and Clevers, H. (1992). Sequence-specific interaction of the HMG box proteins TCF-1 and SRY occurs within the minor groove of a Watson-Crick double helix. EMBO J. 11, 3039-3044.
62. van de Wetering, M., Cavallo, R., Dooijes, D., van Beest, M., van Es, J., Loureiro, J., Ypma, A., Hursh, D., Jones, T., Bejsovec, A. et al. (1997). Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789-799.
63. van Genderen, C., Okamura, R. M., Farinas, I., Quo, R. G., Parslow, T. G., Bruhn, L. and Grosschedl, R. (1994). Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 8, 2691-2703.
64. Vassalli, A., Matzuk, M. M., Gardner, H. A., Lee, K. F. and Jaenisch, R. (1994). Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev. 8, 414-427.
65. Waterman, M. L. (2004). Lymphoid enhancer factor/T cell factor expression in colorectal cancer. Cancer Metastasis. Rev. 23, 41-52.
66. Wirtschafter, J. D., McLoon, L. K., Ketcham, J. M., Weinstock, R. J. and Cheung, J. C. (1997). Palpebral conjunctival transient amplifying cells originate at the mucocutaneous junction and their progeny migrate toward the fornix. Trans. Am. Ophthalmol. Soc. 95, 417-432.
67. Yi, F. and Merrill, B. J. (2007). Stem cells and TCF proteins: a role for betacatenin- independent functions. Stem Cell Rev. 3, 39-48.
68. Yi, F., Pereira, L., Hoffman, J. A., Shy, B. R., Yuen, C. M., Liu, D. R. and Merrill, B. J. (2011). Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat. Cell Biol. 13, 762-770.
69. Zeng, L., Fagotto, F., Zhang, T., Hsu, W., Vasicek, T. J., Perry, W. L., 3rd, Lee, J. J., Tilghman, S. M., Gumbiner, B. M. and Costantini, F. (1997). The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90, 181-192.
70. Zenz, R., Scheuch, H., Martin, P., Frank, C., Eferl, R., Kenner, L., Sibilia, M. and Wagner, E. F. (2003). C-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev. Cell 4, 879-889.
71. Zhang, L., Wang, W., Hayashi, Y., Jester, J. V., Birk, D. E., Gao, M., Liu, C. Y., Kao, W. W., Karin, M. and Xia, Y. (2003). A role for MEK kinase 1 in TGFbeta/activin-induced epithelium movement and embryonic eyelid closure. EMBO J. 22, 4443-4454.
72. Zhou, P., Byrne, C., Jacobs, J. and Fuchs, E. (1995). Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev. 9, 700-713.