Rac1 augments Wnt signaling by stimulating β-catenin-lymphoid enhancer factor-1 complex assembly independent of β-catenin nuclear import

Journal of Cell Science

Volumn 128, Issue 21, 2015, Pages 3933-3946

  Jamieson, Cara ^a   Lui, Christina ^a   Brocardo, Mariana G ^a   Martino Echarri, Estefania ^a   Henderson, Beric R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Proximity ligation assay; Rac1; Wnt signaling; Catenin

Indexed keywords

BETA CATENIN; LYMPHOID ENHANCER FACTOR 1; RAC1 PROTEIN; SERINE; WNT PROTEIN;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELLULAR DISTRIBUTION; COMPLEX FORMATION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; UPREGULATION; WNT SIGNALING PATHWAY; 3T3 CELL LINE; ACTIVE TRANSPORT; ANIMAL; CELL LINE; GENETICS; HCT 116 CELL LINE; METABOLISM; MOUSE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BETA CATENIN; BLOTTING, WESTERN; CELL LINE; HCT116 CELLS; HUMANS; IMMUNOPRECIPITATION; LYMPHOID ENHANCER-BINDING FACTOR 1; MICE; NIH 3T3 CELLS; RAC1 GTP-BINDING PROTEIN; REAL-TIME POLYMERASE CHAIN REACTION; WNT SIGNALING PATHWAY;

EID: 84946031604     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.167742     Document Type: Article

References (51)

1. Behrens, J., von Kries, J. P., Kühl, M., Bruhn, L., Wedlich, D., Grosschedl, R. and Birchmeier, W. (1996). Functional interaction of β-catenin with the transcription factor LEF-1. Nature 382, 638-642.
2. Bikkavilli, R. K., Feigin, M. E. and Malbon, C. C. (2008). Gao mediates WNT-JNK signaling through dishevelled 1 and 3, RhoA family members, and MEKK 1 and 4 in mammalian cells. J. Cell Sci. 121, 234-245.
3. Brabletz, T., Jung, A., Reu, S., Porzner, M., Hlubek, F., Kunz-Schughart, L. A., Knuechel, R. and Kirchner, T. (2001). Variable β-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc. Natl. Acad. Sci. USA 98, 10356-10361.
4. Buongiorno, P., Pethe, V. V., Charames, G. S., Esufali, S. and Bapat, B. (2008). Rac1 GTPase and the Rac1 exchange factor Tiam1 associate with Wntresponsive promoters to enhance β-catenin/TCF-dependent transcription in colorectal cancer cells. Mol. Cancer 7, 73.
5. Chahdi, A. and Raufman, J.-P. (2013). The Cdc42/Rac nucleotide exchange factor protein β1Pix (Pak-interacting exchange factor) modulates β-catenin transcriptional activity in colon cancer cells: evidence for direct interaction of β1PIX with β-catenin. J. Biol. Chem. 288, 34019-34029.
6. Citi, S., Spadaro, D., Schneider, Y., Stutz, J. and Pulimeno, P. (2011). Regulation of small GTPases at epithelial cell-cell junctions. Mol. Membr. Biol. 28, 427-444.
7. Coso, O. A., Chiariello, M., Yu, J.-C., Teramoto, H., Crespo, P., Xu, N., Miki, T. and Gutkind, J. S. (1995). The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
8. Esufali, S. and Bapat, B. (2004). Cross-talk between Rac1 GTPase and dysregulated Wnt signaling pathway leads to cellular redistribution of β-catenin and TCF/LEF-mediated transcriptional activation. Oncogene 23, 8260-8271.
9. Esufali, S., Charames, G. S. and Bapat, B. (2007). Suppression of nuclear Wnt signaling leads to stabilization of Rac1 isoforms. FEBS Lett. 581, 4850-4856.
10. Fritz, G., Just, I. and Kaina, B. (1999). Rho GTPases are over-expressed in human tumors. Int. J. Cancer 81, 682-687.
11. Gao, C., Xiao, G. and Hu, J. (2014). Regulation of Wnt/β-catenin signaling by posttranslational modifications. Cell Biosci. 4, 13.
12. Gómez del Pulgar, T., Benitah, S. A., Valerón, P. F., Espina, C. and Lacal, J. C. (2005). Rho GTPase expression in tumourigenesis: evidence for a significant link. Bioessays 27, 602-613.
13. Gómez del Pulgar, T., Bandrés, E., Espina, C., Valdés-Mora, F., Pérez-Palacios, R., García-Amigot, F., García-Foncillas, J. and Lacal, J. C. (2007). Differential expression of Rac1 identifies its target genes and its contribution to progression of colorectal cancer. Int. J. Biochem. Cell Biol. 39, 2289-2302.
14. Graham, T. A., Clements, W. K., Kimelman, D. and Xu, W. (2002). The crystal structure of the β-catenin/ICAT complex reveals the inhibitory mechanism of ICAT. Mol. Cell 10, 563-571.
15. Habas, R., Dawid, I. B. and He, X. (2003). Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17, 295-309.
16. He, T.-C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B. and Kinzler, K. W. (1998). Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512.
17. Henderson, B. R., Galea, M., Schuechner, S. and Leung, L. (2002). Lymphoid enhancer factor-1 blocks adenomatous polyposis coli-mediated nuclear export and degradation of beta-catenin: regulation by histone deacetylase 1. J. Biol. Chem. 277, 24258-24264.
18. Hovanes, K., Li, T. W., Munguia, J. E., Truong, T., Milovanovic, T., Lawrence Marsh, J., Holcombe, R. F. and Waterman, M. L. (2001). β-Catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat. Genet. 28, 53-57.
19. Huber, O., Korn, R., McLaughlin, J., Ohsugi, M., Herrmann, B. G. and Kemler, R. (1996). Nuclear localization of β-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59, 3-10.
20. Jamieson, C., Sharma, M. and Henderson, B. R. (2011). Regulation of β-catenin nuclear dynamics by GSK-3β involves a LEF-1 positive feedback loop. Traffic 12, 983-999.
21. Jamieson, C., Sharma, M. and Henderson, B. R. (2012). Wnt signaling from membrane to nucleus: β-catenin caught in a loop. Int. J. Biochem. Cell Biol. 44, 847-850.
22. Jamieson, C., Sharma, M. and Henderson, B. R. (2014). Targeting the β-catenin nuclear transport pathway in cancer. Semin. Cancer Biol. 27, 20-29.
23. Jho, E.-H., Zhang, T., Domon, C., Joo, C.-K., Freund, J.-N. and Costantini, F. (2002). Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell Biol. 22, 1172-1183.
24. Johnson, M. A., Sharma, M., Mok, M. T. S. and Henderson, B. R. (2013). Stimulation of in vivo nuclear transport dynamics of actin and its co-factors IQGAP1 and Rac1 in response to DNA replication stress. Biochim. Biophys. Acta 1833, 2334-2347.
25. Kuan, C.-Y., Yang, D. D., Samanta Roy, D. R., Davis, R. J., Rakic, P. and Flavell, R. A. (1999). The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22, 667-676.
26. Lanning, C. C., Ruiz-Velasco, R. and Williams, C. L. (2003). Novel mechanism of the co-regulation of nuclear transport of SmgGDS and Rac1. J. Biol. Chem. 278, 12495-12506.
27. Lanning, C. C., Daddona, J. L., Ruiz-Velasco, R., Shafer, S. H. and Williams, C. L. (2004). The Rac1 C-terminal polybasic region regulates the nuclear localization and protein degradation of Rac1. J. Biol. Chem. 279, 44197-44210.
28. Li, F.-Q., Mofunanya, A., Harris, K. and Takemaru, K.-I. (2008). Chibby cooperates with 14-3-3 to regulate β-catenin subcellular distribution and signaling activity. J. Cell Biol. 181, 1141-1154.
29. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
30. Malliri, A., Rygiel, T. P., van der Kammen, R. A., Song, J.-Y., Engers, R., Hurlstone, A. F. L., Clevers, H. and Collard, J. G. (2006). The rac activator Tiam1 is a Wnt-responsive gene that modifies intestinal tumor development. J. Biol. Chem. 281, 543-548.
31. Mann, B., Gelos, M., Siedow, A., Hanski, M. L., Gratchev, A., Ilyas, M., Bodmer, W. F., Moyer, M. P., Riecken, E. O., Buhr, H. J. et al. (1999). Target genes of β-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc. Natl. Acad. Sci. USA 96, 1603-1608.
32. Michaelson, D., Abidi, W., Guardavaccaro, D., Zhou, M., Ahearn, I., Pagano, M. and Philips, M. R. (2008). Rac1 accumulates in the nucleus during the G2 phase of the cell cycle and promotes cell division. J. Cell. Biol. 181, 485-496.
33. Mosimann, C., Hausmann, G. and Basler, K. (2009). β-Catenin hits chromatin: regulation of Wnt target gene activation. Nat. Rev. Mol. Cell Biol. 10, 276-286.
34. Murga, C., Zohar, M., Teramoto, H. and Gutkind, J. S. (2002). Rac1 and RhoG promote cell survival by the activation of PI3K and Akt, independently of their ability to stimulate JNK and NF-kappaB. Oncogene 21, 207-216.
35. Myant, K. B., Cammareri, P., McGhee, E. J., Ridgway, R. A., Huels, D. J., Cordero, J. B., Schwitalla, S., Kalna, G., Ogg, E.-L., Athineos, D. et al. (2013). ROS production and NF-κB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation. Cell Stem Cell 12, 761-773.
36. Nateri, A. S., Spencer-Dene, B. and Behrens, A. (2005). Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437, 281-285.
37. Perona, R., Montaner, S., Saniger, L., Sanchez-Perez, I., Bravo, R. and Lacal, J. C. (1997). Activation of the nuclear factor-κB by Rho, CDC42, and Rac-1 proteins. Genes Dev. 11, 463-475.
38. Phelps, R. A., Chidester, S., Dehghanizadeh, S., Phelps, J., Sandoval, I. T., Rai, K., Broadbent, T., Sarkar, S., Burt, R. W. and Jones, D. A. (2009). A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137, 623-634.
39. Polakis, P. (2012). Wnt signaling in cancer. Cold Spring Harb. Perspect. Biol. 4, a008052.
40. Sahai, E. and Marshall, C. J. (2002). RHO-GTPases and cancer. Nat. Rev. Cancer 2, 133-142.
41. Schlessinger, K., Hall, A. and Tolwinski, N. (2009). Wnt signaling pathways meet Rho GTPases. Genes Dev. 23, 265-277.
42. Sharma, M. and Henderson, B. R. (2007). IQ-domain GTPase-activating Protein 1 regulates β-catenin at membrane ruffles and its role in macropinocytosis of Ncadherin and adenomatous polyposis coli. J. Biol. Chem. 282, 8545-8556.
43. Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D'Amico, M., Pestell, R. and Ben-Ze'ev, A. (1999). The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA 96, 5522-5527.
44. Söderberg, O., Leuchowius, K.-J., Gullberg, M., Jarvius, M., Weibrecht, I., Larsson, L.-G. and Landegren, U. (2008). Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 45, 227-232.
45. Sparks, A. B., Morin, P. J., Vogelstein, B. and Kinzler, K. W. (1998). Mutational analysis of the APC/β-catenin/Tcf pathway in colorectal cancer. Cancer Res. 58, 1130-1134.
46. Uddin, S., Lekmine, F., Sharma, N., Majchrzak, B., Mayer, I., Young, P. R., Bokoch, G. M., Fish, E. N. and Platanias, L. C. (2000). The Rac1/p38 mitogenactivated protein kinase pathway is required for interferon a-dependent transcriptional activation but not serine phosphorylation of Stat proteins. J. Biol. Chem. 275, 27634-27640.
47. Valenta, T., Hausmann, G. and Basler, K. (2012). The many faces and functions of β-catenin. EMBO J. 31, 2714-2736.
48. Valls, G., Codina, M., Miller, R. K., Del Valle-Perez, B., Vinyoles, M., Caelles, C., McCrea, P. D., Garcia de Herreros, A. and Dunach, M. (2012). Upon Wnt stimulation, Rac1 activation requires Rac1 and Vav2 binding to p120-catenin. J. Cell. Sci. 125, 5288-5301.
49. Wu, X., Tu, X., Joeng, K. S., Hilton, M. J., Williams, D. A. and Long, F. (2008). Rac1 activation controls nuclear localization of β-catenin during canonical Wnt signaling. Cell 133, 340-353.
50. Xu, W. and Kimelman, D. (2007). Mechanistic insights from structural studies of β-catenin and its binding partners. J. Cell. Sci. 120, 3337-3344.
51. Zhao, S.-Y., Sun, Y., Lai, Z.-S., Nan, Q.-Z., Li, K. and Zhang, Z.-S. (2009). Inhibition of migration and invasion of colorectal cancer cells via deletion of Rac1 with RNA interference. Mol. Cell Biochem. 322, 179-184.