Down's-syndrome-related kinase Dyrk1A modulates the p120-catenin-Kaiso trajectory of the Wnt signaling pathway

Journal of Cell Science

Volumn 125, Issue 3, 2012, Pages 561-569

  Hong, Ji Yeon ^a,b   Park, Jae Il ^a   Lee, Moonsup ^a,b   Muñoz, William A ^a,b   Miller, Rachel K ^a   Ji, Hong ^a   Gu, Dongmin ^a,b   Sokol, Sergei Y ^c   McCrea, Pierre D ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Dyrk1A; Hipk; P120 catenin; Siamois; Wnt11

Indexed keywords

BETA CATENIN; DUAL SPECIFICITY TYROSINE REGULATED KINASE 1A; PROTEIN KINASE; PROTEIN P120; SIAMOIS PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR KAISO; UNCLASSIFIED DRUG; WNT PROTEIN; WNT11 PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN SYNDROME; EMBRYO; GASTRULATION; GENE; GENE TARGETING; HUMAN; HUMAN CELL; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CATENINS; DNA PRIMERS; DOWN SYNDROME; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFECTION; WNT SIGNALING PATHWAY; XENOPUS LAEVIS; XENOPUS PROTEINS;

MAMMALIA; XENOPUS LAEVIS;

EID: 84863292131     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.086173     Document Type: Article

References (66)

1. Altafaj, X., Dierssen, M., Baamonde, C., Marti, E., Visa, J., Guimera, J., Oset, M., Gonzalez, J. R., Florez, J., Fillat, C. et al. (2001). Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum. Mol. Genet. 10, 1915-192
2. Anastasiadis, P. Z. (2007). p120-ctn: A nexus for contextual signaling via Rho GTPases. Biochim. Biophys. Acta. 1773, 34-4
3. Anastasiadis, P. Z. and Reynolds, A. B. (2001). Regulation of Rho GTPases by p120-catenin. Curr. Opin. Cell Biol. 13, 604-61
4. Bartlett, J. D., Dobeck, J. M., Tye, C. E., Perez-Moreno, M., Stokes, N., Reynolds, A. B., Fuchs, E. and Skobe, Z. (2010). Targeted p120-catenin ablation disrupts dental enamel development. PLoS One 5, pii:e1270
5. Behrens, J. and Lustig, B. (2004). The Wnt connection to tumorigenesis. Int. J. Dev. Biol. 48, 477-48
6. Bernards, A. and Settleman, J. (2005). GAPs in growth factor signalling. Growth Factors 23, 143-14.
7. Casagolda, D., Del Valle-Perez, B., Valls, G., Lugilde, E., Vinyoles, M., Casado-Vela, J., Solanas, G., Batlle, E., Reynolds, A. B., Casal, J. I. et al. (2010). A p120-catenin-CK1epsilon complex regulates Wnt signaling. J. Cell Sci. 123, 2621-263
8. Cheon, M. S., Shim, K. S., Kim, S. H., Hara, A. and Lubec, G. (2003). Protein levels of genes encoded on chromosome 21 in fetal Down syndrome brain: challenging the gene dosage effect hypothesis (Part IV). Amino Acids 25, 41-4
9. Daniel, J. M. (2007). Dancing in and out of the nucleus: p120(ctn) and the transcription factor Kaiso. Biochim. Biophys. Acta. 1773, 59-6
10. Daniel, J. M. and Reynolds, A. B. (1999). The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol. Cell Biol. 19, 3614-362
11. Daniel, J. M., Spring, C. M., Crawford, H. C., Reynolds, A. B. and Baig, A. (2002). The p120(ctn)-binding partner Kaiso is a bi-modal DNA-binding protein that recognizes both a sequence-specific consensus and methylated CpG dinucleotides. Nucleic Acids Res. 30, 2911-291
12. Davis, M. A. and Reynolds, A. B. (2006). Blocked acinar development, E-cadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev. Cell 10, 21-3
13. Davis, M. A., Ireton, R. C. and Reynolds, A. B. (2003). A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163, 525-53
14. Dohn, M. R., Brown, M. V. and Reynolds, A. B. (2009). An essential role for p120-catenin in Src- and Rac1-mediated anchorage-independent cell growth. J. Cell Biol. 184, 437-45
15. Gu, D., Sater, A. K., Ji, H., Cho, K., Clark, M., Stratton, S. A., Michelle, B. C., Lu, Q. and McCrea, P. D. (2009). Xenopus delta-catenin is expressed widely across developing and adult tissues, is essential in early embryogenesis and is functionally linked to cadherins and small GTPases. J. Cell Sci. 122, 4049-406
16. Fang, X., Ji, H., Kim, S.W., Park, J. I., Vaught, T. G., Anastasiadis, P. Z., Ciesiolka, M. and McCrea, P. D. (2004). Vertebrate development requires ARVCF and p120 catenins and their interplay with RhoA and Rac. J. Cell Biol. 165, 87-9
17. Fotaki, V., Dierssen, M., Alcantara, S., Martinez, S., Marti, E., Casas, C., Visa, J., Soriano, E., Estivill, X. and Arbones, M. L. (2002). Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice. Mol. Cell. Biol. 22, 6636-664
18. Grigoryan, T., Wend, P., Klaus, A. and Birchmeier, W. (2008). Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev. 22, 2308-204
19. Hammerle, B., Carnicero, A., Elizalde, C., Ceron, J., Martinez, S. and Tejedor, F. J. (2003). Expression patterns and subcellular localization of the Down syndrome candidate protein MNB/DYRK1A suggest a role in late neuronal differentiation. Eur. J. Neurosci. 17, 2277-228
20. Hammerle, B., Elizalde, C. and Tejedor, F. J. (2008). The spatio-temporal and subcellular expression of the candidate Down syndrome gene Mnb/Dyrk1A in the developing mouse brain suggests distinct sequential roles in neuronal development. Eur. J. Neurosci. 27, 1061-107
21. Hikasa, H., Ezan, J., Itoh, K., Li, X., Klymkowsky, M. W. and Sokol, S. Y. (2010). Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev. Cell 19, 521-53
22. Himpel, S., Tegge, W., Frank, R., Leder, S., Joost, H. G. and Becker, W. (2000). Specificity determinants of substrate recognition by the protein kinase DYRK1A. J. Biol. Chem. 275, 2431-243
23. Hong, J. Y., Park, J. I., Cho, K., Gu, D., Ji, H., Artandi, S. E. and McCrea, P. D. (2010). Shared molecular mechanisms regulate multiple catenin proteins: canonical Wnt signals and components modulate p120-catenin isoform-1 and additional p120 subfamily members. J. Cell Sci. 123, 4351-436
24. Huelsken, J. and Birchmeier, W. (2001). New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11, 547-55.
25. Iioka, H., Doerner, S. K. and Tamai, K. (2009). Kaiso is a bimodal modulator for Wnt/beta-catenin signaling. FEBS Lett. 583, 627-63
26. Johnson, E., Seachrist, D. D., DeLeon-Rodriguez, C. M., Lozada, K. L., Miedler, J., Abdul-Karim, F. W. and Keri, R. A. (2010). HER2/ErbB2-induced breast cancer cell migration and invasion require p120 catenin activation of Rac1 and Cdc42. J. Biol. Chem. 285, 29491-2950
27. Kelly, K. F., Spring, C. M., Otchere, A. A. and Daniel, J. M. (2004). NLS-dependent nuclear localization of p120ctn is necessary to relieve Kaiso-mediated transcriptional repression. J. Cell Sci. 117, 2675-268
28. Kim, S. W., Fang, X., Ji, H., Paulson, A. F., Daniel, J. M., Ciesiolka, M., van Roy, F. and McCrea, P. D. (2002). Isolation and characterization of XKaiso, a transcriptional repressor that associates with the catenin Xp120(ctn) in Xenopus laevis. J. Biol. Chem. 277, 8202-820
29. Kim, S. W., Park, J. I., Spring, C. M., Sater, A. K., Ji, H., Otchere, A. A., Daniel, J. M. and McCrea, P. D. (2004). Non-canonical Wnt signals are modulated by the Kaiso transcriptional repressor and p120-catenin. Nat. Cell Biol. 6, 1212-122
30. Kim, E. A., Kim, J. E., Sung, K. S., Choi, D. W., Lee, B. J. and Choi, C. Y. (2010). Homeodomain-interacting protein kinase 2 (HIPK2) targets beta-catenin for phosphorylation and proteasomal degradation. Biochem. Biophys. Res. Commun. 394, 966-97
31. Klaus, A. and Birchmeier, W. (2008). Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 8, 387-39
32. Lai, S. L., Chien, A. J. and Moon, R. T. (2009). Wnt/Fz signaling and the cytoskeleton: potential roles in tumorigenesis. Cell Res. 19, 532-54
33. Lee, W., Swarup, S., Chen, J., Ishitani, T. and Verheyen, E. M. (2009). Homeodomain-interacting protein kinases (Hipks) promote Wnt/Wg signaling through stabilization of beta-catenin/Arm and stimulation of target gene expression. Development 136, 241-25
34. 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, 837-84
35. Liu, Y., Dong, Q. Z., Zhao, Y., Dong, X. J., Miao, Y., Dai, S. D., Yang, Z. Q., Zhang, D., Wang, Y., Li, Q. C. et al. (2009). P120-catenin isoforms 1A and 3A differently affect invasion and proliferation of lung cancer cells. Exp. Cell Res. 315, 890-89
36. Louie, S. H., Yang, X. Y., Conrad, W. H., Muster, J., Angers, S., Moon, R. T. and Cheyette, B. N. (2009). Modulation of the beta-catenin signaling pathway by the dishevelled-associated protein Hipk1. PLoS One 4, e431.
37. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-2.
38. Moon, R. T. (2005). Wnt/beta-catenin pathway. Sci. STKE 2005, 271, p. cm.
39. Moon, R. T., Kohn, A. D., De Ferrari, G. V. and Kaykas, A. (2004). WNT and betacatenin signalling: diseases and therapies. Nat. Rev. Genet. 5, 691-70.
40. Mosimann, C., Hausmann, G. and Basler, K. (2009). Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol. Cell Biol. 10, 276-28.
41. Oh, M., Kim, H., Yang, I., Park, J. H., Cong, W. T., Baek, M. C., Bareiss, S., Ki, H., Lu, Q., No, J. et al. (2009). GSK-3 phosphorylates delta-catenin and negatively regulates its stability via ubiquitination/proteosome-mediated proteolysis. J. Biol. Chem. 284, 28579-2858.
42. Okui, M., Ide, T., Morita, K., Funakoshi, E., Ito, F., Ogita, K., Yoneda, Y., Kudoh, J. and Shimizu, N. (1999). High-level expression of the Mnb/Dyrk1A gene in brain and heart during rat early development. Genomics 62, 165-17
43. Park, J. I., Kim, S. W., Lyons, J. P., Ji, H., Nguyen, T. T., Cho, K., Barton, M. C., Deroo, T., Vleminckx, K., Moon, R. T. et al. (2005). Kaiso/p120-catenin and TCF/beta-catenin complexes coordinately regulate canonical Wnt gene targets. Dev. Cell 8, 843-85.
44. Park, J. I., Ji, H., Jun, S., Gu, D., Hikasa, H., Li, L., Sokol, S. Y. and McCrea, P. D. (2006). Frodo links Dishevelled to the p120-catenin/Kaiso pathway: distinct catenin subfamilies promote Wnt signals. Dev. Cell 11, 683-69.
45. Park, J., Song, W. J. and Chung, K. C. (2009). Function and regulation of Dyrk1A: towards understanding Down syndrome. Cell Mol. Life Sci. 66, 3235-324.
46. Perez-Moreno, M., Davis, M. A., Wong, E., Pasolli, H. A., Reynolds, A. B. and Fuchs, E. (2006). p120-catenin mediates inflammatory responses in the skin. Cell 124, 631-64.
47. Perez-Moreno, M., Song, W., Pasolli, H. A., Williams, S. E. and Fuchs, E. (2008). Loss of p120 catenin and links to mitotic alterations, inflammation, and skin cancer. Proc. Natl. Acad. Sci. USA 105, 15399-1540.
48. Prokhortchouk, A., Hendrich, B., Jorgensen, H., Ruzov, A., Wilm, M., Georgiev, G., Bird, A. and Prokhortchouk, E. (2001). The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev. 15, 1613-161.
49. Reynolds, A. B. and Carnahan, R. H. (2004). Regulation of cadherin stability and turnover by p120ctn: implications in disease and cancer. Semin. Cell Dev. Biol. 15, 657-66.
50. Reynolds, A. B. and Roczniak-Ferguson, A. (2004). Emerging roles for p120-catenin in cell adhesion and cancer. Oncogene 23, 7947-795.
51. Ruzov, A., Hackett, J. A., Prokhortchouk, A., Reddington, J. P., Madej, M. J., Dunican, D. S., Prokhortchouk, E., Pennings, S. and Meehan, R. R. (2009a). The interaction of xKaiso with xTcf3: a revised model for integration of epigenetic and Wnt signalling pathways. Development 136, 723-72.
52. Ruzov, A., Savitskaya, E., Hackett, J. A., Reddington, J. P., Prokhortchouk, A., Madej, M. J., Chekanov, N., Li, M., Dunican, D. S., Prokhortchouk, E. et al. (2009b). The non-methylated DNA-binding function of Kaiso is not required in early Xenopus laevis development. Development 136, 729-73.
53. Seifert, A., Allan, L. A. and Clarke, P. R. (2008). DYRK1A phosphorylates caspase 9 at an inhibitory site and is potently inhibited in human cells by harmine. FEBS J. 275, 6268-628.
54. Shi, J., Zhang, T., Zhou, C., Chohan, M. O., Gu, X., Wegiel, J., Zhou, J., Hwang, Y. W., Iqbal, K., Grundke-Iqbal, I. et al. (2008). Increased dosage of Dyrk1A alters alternative splicing factor (ASF)-regulated alternative splicing of tau in Down syndrome. J. Biol. Chem. 283, 28660-2866.
55. Shindoh, N., Kudoh, J., Maeda, H., Yamaki, A., Minoshima, S., Shimizu, Y. and Shimizu, N. (1996). Cloning of a human homolog of the Drosophila Minibrain/rat Dyrk gene from "the Down syndrome critical region of chromosome 21.". Biochem. and Biophys. Res. Commun. 225, 92-9.
56. Smith, D. J., Stevens, M. E., Sudanagunta, S. P., Bronson, R. T., Makhinson, M., Watabe, A. M., O'Dell, T. J., Fung, J., Weier, H. U., Cheng, J. F. et al. (1997). Functional screening of 2 Mb of human chromosome 21q22.2 in transgenic mice implicates minibrain in learning defects associated with Down syndrome. Nat. Genet. 16, 28-3.
57. Song, W. J., Sternberg, L. R., Kasten-Sportes, C., Keuren, M. L., Chung, S. H., Slack, A. C., Miller, D. E., Glover, T. W., Chiang, P. W., Lou, L. et al. (1996). Isolation of human and murine homologues of the Drosophila minibrain gene: human homologue maps to 21q22.2 in the Down syndrome "critical region". Genomics 38, 331-33.
58. Spring, C. M., Kelly, K. F., O'Kelly, I., Graham, M., Crawford, H. C. and Daniel, J. M. (2005). The catenin p120ctn inhibits Kaiso-mediated transcriptional repression of the beta-catenin/TCF target gene matrilysin. Exp. Cell Res. 305, 253-26.
59. Tejedor, F. J. and Hammerle, B. (2010). MNB/DYRK1A as a multiple regulator of neuronal development. FEBS J. 278, 223-23.
60. van Amerongen, R. and Nusse, R. (2009). Towards an integrated view of Wnt signaling in development. Development 136, 3205-321.
61. van Roy, F. M. and McCrea, P. D. (2005). A role for Kaiso-p120ctn complexes in cancer? Nat. Rev. Cancer 5, 956-96.
62. Verheyen, E. M. and Gottardi, C. J. (2010). Regulation of Wnt/beta-catenin signaling by protein kinases. Dev. Dyn. 239, 34-4.
63. Wegiel, J., Gong, C. X. and Hwang, Y. W. (2010). The role of DYRK1A in neurodegenerative diseases. FEBS J. 278, 236-245.
64. Wend, P., Holland, J. D., Ziebold, U. and Birchmeier, W. (2010). Wnt signaling in stem and cancer stem cells. Semin. Cell Dev. Biol. 21, 855-86
65. Wildenberg, G. A., Dohn, M. R., Carnahan, R. H., Davis, M. A., Lobdell, N. A., Settleman, J. and Reynolds, A. B. (2006). p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127, 1027-103.
66. Xiao, K., Oas, R. G., Chiasson, C. M. and Kowalczyk, A. P. (2007). Role of p120-catenin in cadherin trafficking. Biochim. Biophys. Acta. 1773, 8-1.