Skip to main content

Advertisement

SpringerLink
Log in

Stem Cells and TCF Proteins: A Role for β-Catenin—Independent Functions

  • Published:
Stem Cell Reviews Aims and scope Submit manuscript

Abstract

The Wnt signal transduction pathway has been shown to stimulate stem cell self renewal and has been shown to cause cancer in humans. One interesting aspect of Wnt signaling is that it utilizes downstream DNA-binding transcription factors, called Tcf proteins, which can activate transcription of target genes in the presence of a Wnt signal and repress the expression of target genes in the absence of a Wnt signal. Since Tcf proteins are present in Wnt-stimulated and unstimulated stem cells, understanding how Tcf proteins regulate target gene expression in each state offers the potential to understand how stem cells regulate their self-renewal, differentiation, and proliferation. In this article, we will review recent work elucidating the roles Tcf-protein interactions in the context of stem cells and cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Morrison, S. J., Wandycz, A. M., Akashi, K., Globerson, A., & Weissman I. L. (1996). The aging of hematopoietic stem cells. Natral Medicine, 2, 1011–1016.

    Article  CAS  Google Scholar 

  2. Rossi, D. J., Bryder, D., Zahn, J. M., Ahlenius, H., Sonu, R., Wagers, A. J., et al. (2005). Cell intrinsic alterations underlie hematopoietic stem cell aging. Proceedings of the National Academy of Sciences of the United States of America, 102, 9194–9199.

    Article  PubMed  CAS  Google Scholar 

  3. Beachy, P. A., Karhadkar, S. S., & Berman, D. M. (2004). Tissue repair and stem cell renewal in carcinogenesis. Nature, 432, 324–331.

    Article  PubMed  CAS  Google Scholar 

  4. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J., & Clarke, M. F. (2003). Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 3983–3988.

    Article  PubMed  CAS  Google Scholar 

  5. Bonnet, D., & Dick, J. E. (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Natural Medicines, 3, 730–737.

    Article  CAS  Google Scholar 

  6. Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J., et al. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Research, 63, 5821–5828.

    PubMed  CAS  Google Scholar 

  7. Singh, S. K., Hawkins, C., Clarke, I. D., Squire, J. A., Bayani, J., Hide, T., et al. (2004). Identification of human brain tumour initiating cells. Nature, 432, 396–401.

    Article  PubMed  CAS  Google Scholar 

  8. van Amerongen, R., & Berns, A. (2006). Knockout mouse models to study Wnt signal transduction. Trends in Genetics, 22, 678–689.

    Article  PubMed  CAS  Google Scholar 

  9. Arce, L., Yokoyama, N. N., & Waterman, M. L. (2006). Diversity of LEF/TCF action in development and disease. Oncogene, 25, 7492–7504.

    Article  PubMed  CAS  Google Scholar 

  10. Clevers, H. (2006). Wnt/β-catenin signaling in development and disease. Cell, 127, 469–480.

    Article  PubMed  CAS  Google Scholar 

  11. Kimelman, D., & Xu, W. (2006). The β-catenin destruction complex: Insights and questions from a structural perspective (review). Oncogene, 25, 7482–7491.

    Article  PubMed  CAS  Google Scholar 

  12. Mikels, A. J., & Nusse, R. (2006). Wnt as ligands: Processing, secretion and reception. Oncogene, 25, 7461–7468.

    Article  PubMed  CAS  Google Scholar 

  13. Takemaru, K. I., & Moon, R. T. (2000). The transcriptional coactivator CBP interacts with beta-catenin to active gene expression. Journal of Cell Biology, 149, 249–254.

    Article  PubMed  CAS  Google Scholar 

  14. Hecht, A., Vleminckx, K., Stemmler, M. P., van Roy, F., & Kemler, R. (2000). The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates. EMBO Journal, 19, 1839–1850.

    Article  PubMed  CAS  Google Scholar 

  15. Barker, N., Hurlstone, A., Musisi, H., Miles, A., Bienz, M., & Clevers, H. (2001). The chromatin remodeling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO Journal, 20, 4935–4943.

    Article  PubMed  CAS  Google Scholar 

  16. Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., et al. (2002). Wnt/Wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell, 109, 47–60.

    Article  PubMed  CAS  Google Scholar 

  17. Reya, T., Duncan, A. W., Ailles, L., Domen, J., Scherer, D. C., Willert, K., et al. (2003). A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature, 423, 409–414.

    Article  PubMed  CAS  Google Scholar 

  18. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., et al. (2003). Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature, 423, 448–452.

    Article  PubMed  CAS  Google Scholar 

  19. Van Mater, D., Kolligs, F. T., Dlugosz, A. A., & Fearon, E. R. (2003). Transient activation of beta-catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes & Development, 17, 1219–1224.

    Article  CAS  Google Scholar 

  20. Gat, U., DasGupta, R., Degenstein, L., & Fuchs, E. (1998). De Novo hair follicles morphogenesis and hair tumors in mice expressing a truncated β-catenin in skin. Cell, 95, 605–614.

    Article  PubMed  CAS  Google Scholar 

  21. Blanpain, C., Lowry, W. E., Geoghegan, A., Polak, L., & Fuchs, E. (2004). Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell, 118, 635–648.

    Article  PubMed  CAS  Google Scholar 

  22. Lowry, W. E., Blanpain, C., Nowak, J. A., Guasch, G., Lewis, L., & Fuchs, E. (2005). Defining the impact of β-catenin/TCF transactivation on epithelial stem cells. Genes & Development, 19, 1596–1611.

    Article  CAS  Google Scholar 

  23. van de Wetering, M., Sancho, E., Verweij, C., de Lau, W., Oving, I., Hurlstone, A., et al. (2002). The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell, 111, 241–250.

    Article  PubMed  Google Scholar 

  24. Sansom, O. J., Reed, K. R., Hayes, A. J., Ireland, H., Brinkmann, H., Newton, I. P., et al. (2004). Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes & Development, 18, 1385–1390.

    Article  CAS  Google Scholar 

  25. Nusse, R., van Ooyen, A., Cox, D., Fung, Y. K., & Varmus, H. (1984). Mode of proviral activation of a putative mammary oncogene (int-1) on mouse chromosome 15. Nature, 307, 131–136.

    Article  PubMed  CAS  Google Scholar 

  26. Kinzler, K. W., & Vogelstein B. (1996). Lessons from hereditary colorectal cancer. Cell, 87, 159–170.

    Article  PubMed  CAS  Google Scholar 

  27. Morin, P. J. (1999). Beta-catenin signaling and cancer. Bioessays, 21, 1021–1030.

    Article  PubMed  CAS  Google Scholar 

  28. Simon, M., Grandage, V. L., Linch, D. C., Khwaja, A. (2005). Constitutive activation of the Wnt/β-catenin signalling pathway in acute myeloid leukemia. Oncogene, 24, 2410–2420.

    Article  PubMed  CAS  Google Scholar 

  29. Coluccia, A. M., Vacca, A., Dunach, M., Mologni, L., Redaelli, S., Bustos, V. H., et al. (2007). Bcr-Abl stabilizes beta-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO Journal, 26, 1456–1466.

    Article  PubMed  CAS  Google Scholar 

  30. Muller-Tidow, C., Steffen, B., Cauvet, T., Tickenbrock, L., Ji, P., Diederichs, S., et al. (2004). Translocation products in acute myeloid leukemia activate the Wnt signaling in hematopoietic cells. Molecular and Cellular Biology, 24, 2890–2904.

    Article  PubMed  CAS  Google Scholar 

  31. Tetsu, O., & McCormick, F. (1999). β-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature, 398, 422–426.

    Article  PubMed  CAS  Google Scholar 

  32. He, T. C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., et al. (1998). Identification of c-MYC as a target of the APC pathway. Science, 281, 1509–1512.

    Article  PubMed  CAS  Google Scholar 

  33. Roose, J., Huls, G., van Beest, M., Moerer, P., van der Horn, K., Goldschmeding, R., et al. (1999). Synergy between tumor suppressor APC and the beta-catenin Tcf4 target Tcf1. Science, 285, 1923–1926.

    Article  PubMed  CAS  Google Scholar 

  34. Roose, J., & Clevers H., (1999). TCF transcription factors: Molecular switches in carcinogenesis. Biochimica et Biophysica Acta, 1424, M23–37.

    PubMed  CAS  Google Scholar 

  35. Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., et al. (2003). Mapping Wnt/beta-catenin signaling mouse development and in colorectal tumors. Proceedings of the National Academy of Sciences of the United States of America, 100, 3299–3304.

    Article  PubMed  CAS  Google Scholar 

  36. Daniels, D. L., & Weis, W. I. (2005). Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nature Structural and Molecular Biology, 12, 364–371.

    Article  PubMed  CAS  Google Scholar 

  37. Roose, J., Molenaar, M., Peterson, J., Hurenkamp, J., Brantjes, H., Moerer, P., et al. (1998). The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature, 395, 608–612.

    Article  PubMed  CAS  Google Scholar 

  38. Cavallo, R. A., Cox, R. T., Moline, M. M., Roose, J., Polevoy, G. A., Clevers, H., et al. (1998). Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature, 395, 604–608.

    Article  PubMed  CAS  Google Scholar 

  39. Brantjes, H., Roose, J., van De Wetering, M., & Clevers, H. (2001). All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Research, 29, 1410–1419.

    Article  PubMed  CAS  Google Scholar 

  40. Tutter, A. V., Fryer, C. J., & Jones, K. A. (2001). Chromatin-specific regulation of LEF-1 beta-catenin transcription activation and inhibition in vitro. Genes & Development, 15, 3342–3354.

    Article  CAS  Google Scholar 

  41. Atcha, F. A., Munguia, J. E., Li, T. W., Hovanes, K., & Waterman, M. L., (2003). A new beta-catenin-dependent activation domain in T cell factor. Journal of Biological Chemistry, 278, 16169–16175.

    Article  PubMed  CAS  Google Scholar 

  42. Hovanes, K., Li, T. W., Munguia, J. E., Truong, T., Milovanovic, T., Lawrence Marsh, J., et al. (2001). Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nature Genetics, 28, 53–57.

    Article  PubMed  CAS  Google Scholar 

  43. Li, T. W., Ting, J. H., Yokoyama, N. N., Bernstein, A., van de Wetering, M., & Waterman, M. L. (2006). Wnt activation and alternative promoter regression of LEF 1 in colon cancer. Molecular and Cellular Biology, 26, 5284–5299.

    Article  PubMed  CAS  Google Scholar 

  44. Shulewitz, M., Soloviev, I., Wu, T., Koeppen, H., Polakis, P., & Sakanaka C. (2006). Repressor roles for TCF-4 and Sfrp1 in Wnt signaling in breast cancer. Oncogene, 25(31), 4361–4369.

    Google Scholar 

  45. Ivanova, N. B., Dimos, J. T., Schaniel, C., Hackney, J. A., Moore, K. A., & Lemischka, I. R. (2002). A stem cell molecular signature. Science, 298, 601–604.

    Article  PubMed  CAS  Google Scholar 

  46. Merrill, B. J., Gat, U., DasGupta, R., & Fuchs, E. (2001). Lef-1 and Tcf-3 transcription factors mediate tissue specific Wnt signaling during Xenopus development. Genes & Development, 15, 1688–1705.

    Article  CAS  Google Scholar 

  47. Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M., et al. (2004). Defining the epithelial stem cell niche in skin. Science, 303, 359–363.

    Article  PubMed  CAS  Google Scholar 

  48. DasGupta, R., & Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development, 126, 4557–4568.

    PubMed  CAS  Google Scholar 

  49. Kim, C. H., Oda, T., Itoh, M., Jiang, D., Artinger, K. B., Chandrasekharappa, S. C., et al. (2000). Repressor activity of Headless/TCF-3 is essential for vertebrate head formation. Nature, 407, 913–916.

    Article  PubMed  CAS  Google Scholar 

  50. Roel, G., Hamilton, F. S., Gent, Y., Bain, A. A., Destree, O., & Hoppler, S. (2002). LEF-1 and Tcf-3 transcription factors mediate tissue-specific Wnt signaling during Xenopus development. Current Biology, 12, 1941–1945.

    Article  PubMed  CAS  Google Scholar 

  51. Nguyen, H., Rendl, M., & Fuchs, E. (2006). Tcf-3 governs stem cell features and represses cell fate determination in skin. Cell, 127, 171–183.

    Article  PubMed  CAS  Google Scholar 

  52. Rendl, M., Lewis, L., & Fuchs, E. (2005). Molecular dissection of mesenchymal-epithelial interactions in the hair follicle. PLoS Biology, 3, e331.

    Article  PubMed  CAS  Google Scholar 

  53. Blanpain, C., & Fuchs, E. (2006). Epidermal stem cells of the skin. Annual Review of Cell and Develpment Biology, 22, 339–373.

    Article  CAS  Google Scholar 

  54. Chazaud, C., & Rossant, J. (2006). Disruption of early proximodistal patterning and AVE formation in APC mutants. Development, 133, 3379–3387.

    Article  PubMed  CAS  Google Scholar 

  55. Perea-Gomez, A., Vella, F. D., Shawlot, W., Oulad-Abdelghani, M., Chazaud, C., Meno, C., et al. (2002). Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Developmental Cell, 3, 745–756.

    Article  PubMed  CAS  Google Scholar 

  56. Merrill, B. J., Pasolli, H. A., Polak, L., Rendl, M., Garcia-Garcia, M. J., Anderson, K. V., et al. (2004). Tcf3: A transcriptional regulator of axis reduction in the early embryo. Development, 131, 263–274.

    Article  PubMed  CAS  Google Scholar 

  57. Popperl, H., Schmidt, C., Wilson, V., Hume, C. R., Dodd, J., Krumlauf, R., et al. (1997). Misexpression of CWnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm. Development, 124, 2997–3005.

    PubMed  CAS  Google Scholar 

  58. Ishikawa, T. O., Tamai, Y., Li, Q., Oshima, M., & Taketo, M. M. (2003). Requirement for tumor suppressor APC in the morphogenesis of anterior and ventral mouse embryo. Developmental Biology, 253, 230–246.

    Article  PubMed  CAS  Google Scholar 

  59. Zeng, L., Fagotto, F., Zhang, T., Hsu, W., Vasicek, T. J., Perry 3rd, W. L., et al. (1997). The mouse fused locus encodes axis, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell, 90, 181–192.

    Article  PubMed  CAS  Google Scholar 

  60. Pereira, L., Yi, F., & Merrill, B. J. (2006). Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Molecular and Cellular Biology, 26, 7479–7491.

    Article  PubMed  CAS  Google Scholar 

  61. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S., et al. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell, 113, 643–655.

    Article  PubMed  CAS  Google Scholar 

  62. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., et al. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell, 113, 631–642.

    Article  PubMed  CAS  Google Scholar 

  63. Ying, Q. L., Nichols, J., Chambers, I., & Smith, A. (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboartion with STAT3. Cell, 115, 281–292.

    Article  PubMed  CAS  Google Scholar 

  64. Kuroda, T., Tada, M., Kubota, H., Kimura, H., Hatano, S. Y., Suemori, H., et al. (2005). Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Molecular and Cellular Biology, 25, 2475–2485.

    Article  PubMed  CAS  Google Scholar 

  65. Rodda, D. J., Chew, J. L., Lim, L. H., Loh, Y. H., Wang, B., Ng, H. H., et al. (2005). Transcriptional regulation of Nanog by OCT4 and SOX4. Journal of Biological Chemistry, 280, 24731–24737.

    Article  PubMed  CAS  Google Scholar 

  66. Wu da, Y., & Yao, Z. (2005). Isolation and characterization of the murine Nanog gene promoter. Cell Research, 15, 317–324.

    Article  PubMed  Google Scholar 

  67. Monk, M., & Holding, C. (2001). Human embryonic genes re-expressed in cancer cells. Oncogene, 20, 8085–8091.

    Article  PubMed  CAS  Google Scholar 

  68. Hochedlinger, K., Yamada, Y., Beard, C., & Jaenisch, R. (2005). Ectopic expression of OCT4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell, 121, 465–477.

    Article  PubMed  CAS  Google Scholar 

  69. Zhang, J., Wang, X., Chen, B., Suo, G., Zhao, Y., Duan, Z., et al. (2005). Expression of Nanog gene promotes NIH3T3 cell proliferation. Biochemical and Biophysical Research Comunications, 338, 1098–1102.

    Article  CAS  Google Scholar 

  70. Piestun, D., Kochupurakkal, B. S., Jacob-Hirsch, J., Zeligson, S., Koudritsky, M., Domany, E., et al. (2006). Nanog transformed NIH3T3 cell and targets cell-type restricted genes. Biochemical and Biophysical Research Comunications, 343(1), 279–285.

    Google Scholar 

  71. Clark, A. T., Rodriguez, R. T., Bodnar, M. S., Abeyta, M. J., Cedars, M. I., Turek, P. J., et al. (2004). Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma. Stem Cells, 22, 169–179.

    Article  PubMed  CAS  Google Scholar 

  72. Ezeh, U. I., Turek, P.J., Reijo, R. A., & Clark, A. T. (2005). Human embryonic stem cell genes OCT4, NANOG, STELLAR, and GDF3 are expressed in both seminoma and breast carcinoma. Cancer, 104(104), 2255–2265.

    Google Scholar 

  73. Gibbs, C. P., Kukekov, V. G., Reith, J. D., Tchigrinova, O., Suslov, O. N., Scott, E. W., et al. (2005). Stem-like cells in bone sarcomas: Implications for tumorigenesis. Neoplasia, 7, 967–976.

    Article  PubMed  CAS  Google Scholar 

  74. Miravet, S., Piedra, J., Miro, F., Itarte, E., Garcia de Herreros, A., & Dunach, M. (2002). The transcriptional factor Tcf-4 contains different binding sites for beta-catenin and plakoglobin. Journal of Biological Chemistry, 277, 1884–1891.

    Article  PubMed  CAS  Google Scholar 

  75. Vadlamudi, U., Espinoza, H. M., Ganga, M., Martin, D. M., Liu, X., Engelhardt, J. F., et al. (2005). PITX2, beta-catenin and LEF-1 interact to synergistically regulate the LEF-1 promoter. Journal of Cell Science, 118, 1129–1137.

    Article  PubMed  CAS  Google Scholar 

  76. Sheridan, P. L., Sheline, C. T., Cannon, K., Voz, M. L., Pazin, M. J., Kadonaga, J. T., et al. (1995). Activation of the HIV-1 enhancer by the LEF-1 HMG protein on nucleosome-assembled DNA in vitro. Genes & Development, 9, 2090–2104.

    Article  CAS  Google Scholar 

  77. Giese, K., Kingsley, C., Kirshner, J. R., & Grosschedl, R. (1995). Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein–protein interactions. Genes & Development, 9, 995–1008.

    Article  CAS  Google Scholar 

  78. Carlsson, P., Waterman, M. L., & Jones, K. A. (1993). The hLEF/TCF-1 alpha HMG protein contains a context-dependent transcriptional activation domain that induces the TCR alpha enhancer in T cells. Genes & Development, 7, 2418–2430.

    Article  CAS  Google Scholar 

  79. Yasumoto, K., Takeda, K., Saito, H., Watanabe, K., Takahashi, K., & Shibahara, S. (2002). Microphthalmia-associated transcription factor interacts with LEF-1, a mediator of Wnt signaling. EMBO Journal, 21, 2703–2714.

    Article  PubMed  CAS  Google Scholar 

  80. Bruhn, L., Munnerlyn, A., & Grosschedl, R. (1997). ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCR alpha enhancer function. Genes & Development, 11, 640–653.

    Article  CAS  Google Scholar 

  81. Ghogomu, S. M., van Venrooy, S., Ritthaler, M., Wedlich, D., & Gradl, D. (2006). HIC-5 is a novel repressor of lymphoid enhancer factor/T-cell factor-driven transcription. Journal of Biological Chemistry, 281, 1755–1764.

    Article  PubMed  CAS  Google Scholar 

  82. Pukrop, T., Gradl, D., Henningfeld, K. A., Knochel, W., Wedlich, D., & Kuhl, M. (2001). Identification of two regulatory elements within the high mobility group box transcription factor XTCF-4. Journal of Biological Chemistry, 276, 8968–8978.

    Article  PubMed  CAS  Google Scholar 

  83. Nishita, M., Hashimoto, M. K., Ogata, S., Laurent, M. N., Ueno, N., Shibuya, H., et al. (2000). Interaction between Wnt and TGF-β signalling pathways during formation of Spemann’s organizers. Nature, 403, 781–785.

    Article  PubMed  CAS  Google Scholar 

  84. Labbe, E., Letamendia, A., & Attisano, L. (2000). Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-β and Wnt pathways. Proceedings of the National Academy of Sciences of the United States of America, 97, 8358–8363.

    Article  PubMed  CAS  Google Scholar 

  85. Boras, K., & Hamel, P. A. (2002). Alx4 binding to LEF-1 regulates N-CAM promoter activity. Journal of Biological Chemistry, 277, 1120–1127.

    Article  PubMed  CAS  Google Scholar 

  86. Kahler, R. A., & Westendorf, J. J. (2003). Lymphoid enhancer factor-1 and beta-catenin inhibit Runx2-dependent transcriptional activation of the osteocalcin promoter. Journal of Biological Chemistry, 278, 11937–11944.

    Article  PubMed  CAS  Google Scholar 

  87. Valenta, T., Lukas, J., Doubravska, L., Fafilek, B., & Korinek, V. (2006). HIC1 attenuates Wnt signaling by recruitment of TCF-4 and beta-catenin to the nuclear bodies. EMBO Journal, 25, 2326–2337.

    Article  PubMed  CAS  Google Scholar 

  88. Kusano, S., & Raab-Traub, N. (2002). I-mfa domain proteins interact with axin and affect its regulation of the Wnt and c-Jun N-terminal kinase signaling pathways. Molecular and Cellular Biology, 22, 6393–6405.

    Article  PubMed  CAS  Google Scholar 

  89. Prieve, M. G., Guttridge, K. L., Munguia, J., Waterman, M. L. (1998). Differential importin- recognition and nuclear transport by nuclear localization signals within the high-mobility-group DNA binding domains of lymphoid enhancer factor 1 and T-cell factor 1. Molecular and Cellular Biology, 18, 4819–4832.

    PubMed  CAS  Google Scholar 

  90. Beland, M., Pilon, N., Houle, M., Oh, K., Sylvestre, J. R., Prinos, P., et al. (2004). Cdx1 autoregulation is governed by a novel Cdx1-LEF1 transcription complex. Molecular and Cellular Biology, 24, 5028–5038.

    Article  PubMed  CAS  Google Scholar 

  91. Brannon, M., Brown, J. D., Bates, R., Kimelman, D., & Moon, R. T. (1999). XCtBP is a XTct-3 co-repressor with roles throughout Xenopus development. Development, 126, 3159–3170.

    PubMed  CAS  Google Scholar 

  92. Park, J. I., Kim, S. W., Lyons, J. P., Ji, H., Nguyen, T. T., Cho, K., et al. (2005). Kaiso/p120-catenin and TCF/β-catenin complexes coordinately regulate canonical Wnt gene targets. Developmental Cell, 8, 843–854.

    Article  PubMed  CAS  Google Scholar 

  93. Hikasa, H., & Sokol, S. Y. (2004). The involvement of Frodo in TCF-dependent signaling and neural tissue development. Development, 131, 4725–4734.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank the members of the Merrill Lab (Laura Pereira, Jackson Hoffman, and Travis Leonard) for helpful discussions concerning the topics presented in this review. B.J.M. was supported by awards from the Stem Cell Research Foundation, Schweppe Foundation, and the American Cancer Society—Illinois Division.

Author information

Authors and Affiliations

  1. Room 1268, Molecular Biology Research Building, Department of Biochemistry and Molecular Genetics, University of Illinois, 900 S. Ashland Ave., 669, Chicago, IL, 60607, USA

    Fei Yi & Bradley J. Merrill

Authors
  1. Fei Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bradley J. Merrill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bradley J. Merrill.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yi, F., Merrill, B.J. Stem Cells and TCF Proteins: A Role for β-Catenin—Independent Functions. Stem Cell Rev 3, 39–48 (2007). https://doi.org/10.1007/s12015-007-0003-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12015-007-0003-9

Keywords

Search

Navigation