The postsynaptic density 95/disc-large/zona occludens protein syntenin directly interacts with Frizzled 7 and supports noncanonical Wnt signaling

Molecular Biology of the Cell

Volumn 19, Issue 4, 2008, Pages 1594-1604

  Luyten, Annouck ^a,b   Mortier, Eva ^a,b   Van Campenhout, Claude ^c   Taelman, Vincent ^c   Degeest, Gisèle ^a,b   Wuytens, Gunther ^a,b   Lambaerts, Kathleen ^a,b   David, Guido ^a,b   Bellefroid, Eric J ^c   Zimmermann, Pascale ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DISHEVELLED PROTEIN; FRIZZLED PROTEIN; PROTEIN CDC42; PROTEIN KINASE C ALPHA; STRESS ACTIVATED PROTEIN KINASE; SYNDECAN; SYNTENIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CELLS, CULTURED; DNA, COMPLEMENTARY; FEMALE; FRIZZLED RECEPTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; STAT1 TRANSCRIPTION FACTOR; SURFACE PLASMON RESONANCE; SYNDECANS; SYNTENINS; WNT PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 44949220276     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-08-0832     Document Type: Article

References (57)

1. Ataman, B., Ashley, J., Gorczyca, D., Gorczyca, M., Mathew, D., Wichmann, C., Sigrist, S. J., and Budnik, V. (2006). Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc. Natl. Acad. Sci. USA 103, 7841-7846.
2. Bellefroid, E. J., Bourguignon, C., Hollemann, T., Ma, Q., Anderson, D. J., Kintner, C., and Pieler, T. (1996). X-MyT1, a Xenopus C2HC-type zinc finger protein with a regulatory function in neuronal differentiation. Cell 87, 1191-1202.
3. Billin, A. N., Thirlwell, H., and Ayer, D. E. (2000). Beta-catenin-histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Mol. Cell. Biol. 20, 6882-6890.
4. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007). Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037.
5. Boukerche, H., Su, Z. Z., Emdad, L., Baril, P., Balme, B., Thomas, L., Randolph, A., Valerie, K., Sarkar, D., and Fisher, P. B. (2005). mda-9/Syntenin: a positive regulator of melanoma metastasis. Cancer Res. 65, 10901-10911.
6. Boutros, M., and Mlodzik, M. (1999). Dishevelled: at the crossroads of divergent intracellular signaling pathways. Mech. Dev. 83, 27-37.
7. Boutros, M., Paricio, N., Strutt, D. I., and Mlodzik, M. (1998). Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109-118.
8. 2+ signaling pathway. Dev. Biol. 244, 342-357.
9. Couchman, J. R. (2003). Syndecans: proteoglycan regulators of cell-surface microdomains? Nat. Rev. Mol. Cell Biol. 4, 926-937.
10. Darken, R. S., Scola, A. M., Rakeman, A. S., Das, G., Mlodzik, M., and Wilson, P. A. (2002). The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J. 21, 976-985.
11. Dissanayake, S. K. et al. (2007). The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J. Biol. Chem. 282, 17259-17271.
12. Djiane, A., Riou, J., Umbhauer, M., Boucaut, J., and Shi, D. (2000). Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 127, 3091-3100.
13. Djiane, A., Yogev, S., and Mlodzik, M. (2005). The apical determinants aPKC and dPatj regulate Frizzled-dependent planar cell polarity in the Drosophila eye. Cell 121, 621-631.
14. Fujii, N. et al. (2007). An antagonist of dishevelled protein-protein interaction suppresses beta-catenin-dependent tumor cell growth. Cancer Res. 67, 573-579.
15. Granes, F., Garcia, R., Casaroli-Marano, R. P., Castel, S., Rocamora, N., Reina, M., Urena, J. M., and Vilaro, S. (1999). Syndecan-2 induces filopodia by active cdc42Hs. Exp. Cell Res. 248, 439-456.
16. Grootjans, J. J., Reekmans, G., Ceulemans, H., and David, G. (2000). Syntenin-syndecan binding requires syndecan-synteny and the co-operation of both PDZ domains of syntenin. J. Biol. Chem. 275, 19933-19941.
17. Grootjans, J. J., Zimmermann, P., Reekmans, G., Smets, A., Degeest, G., Durr, J., and David, G. (1997). Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci. USA 94, 13683-13688.
18. Johnson, M. L., and Rajamannan, N. (2006). Diseases of Wnt signaling. Rev. Endocr. Metab. Disord. 7, 41-49 [correction published in Rev. Endocr. Metab. Disord (2007) 8, 183].
19. Katoh, M. (2005). WNT/PCP signaling pathway and human cancer (review). Oncol. Rep. 14, 1583-1588.
20. Kohn, A. D., and Moon, R. T. (2005). Wnt and calcium signaling: beta-cateninin-dependent pathways. Cell Calcium 38, 439-446.
21. Koo, T. H., Lee, J. J., Kim, E. M., Kim, K. W., Kim, H. D., and Lee, J. H. (2002). Syntenin is overexpressed and promotes cell migration in metastatic human breast and gastric cancer cell lines. Oncogene 21, 4080-4088.
22. 2+ signaling. Mech. Dev. 106, 61-76.
23. Lim, S. T., Longley, R. L., Couchman, J. R., and Woods, A. (2003). Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase C alpha (PKC alpha) increases focal adhesion localization of PKC alpha. J. Biol. Chem. 278, 13795-13802.
24. Logan, C. Y., and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
25. Margolis, B., and Borg, J. P. (2005). Apicobasal polarity complexes. J. Cell Sci. 118, 5157-5159.
26. Medina, A., Reintsch, W., and Steinbeisser, H. (2000). Xenopus frizzled 7 can act in canonical and non-canonical Wnt signaling pathways: implications on early patterning and morphogenesis. Mech. Dev. 92, 227-237.
27. Meerschaert, K., Bruyneel, E., De Wever, O., Vanloo, B., Boucherie, C., Bracke, M., Vandekerckhove, J., and Gettemans, J. (2007). The tandem PDZ domains of syntenin promote cell invasion. Exp. Cell Res. 313, 1790-1804.
28. Mortier, E., Wuytens, G., Leenaerts, I., Hannes, F., Heung, M. Y., Degeest, G., David, G., and Zimmermann, P. (2005). Nuclear speckles and nucleoli targeting by PIP2-PDZ domain interactions. EMBO J. 24, 2556-2565.
29. Munoz, R., Moreno, M., Oliva, C., Orbenes, C., and Larrain, J. (2006). Syndecan-4 regulates non-canonical Wnt signalling and is essential for convergent and extension movements in Xenopus embryos. Nat. Cell Biol. 8, 492-500.
30. Nieuwkoop, P. D., and Faber J. (1967). A Laboratory Manual, Amsterdam, The Netherlands: North Holland Publishing Company.
31. Nourry, C., Grant, S. G., and Borg, J. P. (2003). PDZ domain proteins: plug and play! Sci. STKE 2003, RE7.
32. Oh, E. S., Woods, A., Lim, S. T., Theibert, A. W., and Couchman, J. R. (1998). Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate coordinately regulate protein kinase C activity. J. Biol. Chem. 273, 10624-10629.
33. Penzo-Mendez, A., Umbhauer, M., Djiane, A., Boucaut, J. C., and Riou, J. F. (2003). Activation of Gbetagamma signaling downstream of Wnt-11/Xfz7 regulates Cdc42 activity during Xenopus gastrulation. Dev. Biol. 257, 302-314.
34. Polakis, P. (2000). Wnt signaling and cancer. Genes Dev. 14, 1837-1851.
35. Reichsman, F., Smith, L., and Cumberledge, S. (1996). Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction. J. Cell Biol. 135, 819-827.
36. Shan, J., Shi, D. L., Wang, J., and Zheng, J. (2005). Identification of a specific inhibitor of the dishevelled PDZ domain. Biochemistry 44, 15495-15503.
37. 2+ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161, 769-777.
38. Shibata, M., Itoh, M., Hikasa, H., Taira, S., and Taira, M. (2005). Role of crescent in convergent extension movements by modulating Wnt signaling in early Xenopus embryogenesis. Mech. Dev. 122, 1322-1339.
39. Sive, H. L., Grainer R. M., Harland R. M. (2000). A laboratory manual. Cold Spring Harbor, Laboratory Press: Cold Spring Harbor, NY.
40. Strutt, D. (2003). Frizzled signalling and cell polarisation in Drosophila and vertebrates. Development 130, 4501-4513.
41. Sumanas, S., and Ekker, S. C. (2001). Xenopus frizzled-7 morphant displays defects in dorsoventral patterning and convergent extension movements during gastrulation. Genesis 30, 119-122.
42. Tada, M., and Smith, J. C. (2000). Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127, 2227-2238.
43. Tan, C., Deardorff, M. A., Saint-Jeannet, J. P., Yang, J., Arzoumanian, A., and Klein, P. S. (2001). Kermit, a frizzled interacting protein, regulates frizzled 3 signaling in neural crest development. Development 128, 3665-3674.
44. Umbhauer, M., Djiane, A., Goisset, C., Penzo-Mendez, A., Riou, J. F., Boucaut, J. C., and Shi, D. L. (2000). The C-terminal cytoplasmic Lys-thr-X-X-X-Trp motif in frizzled receptors mediates Wnt/beta-catenin signalling. EMBO J. 19, 4944-4954.
45. Veeman, M. T., Axelrod, J. D., and Moon, R. T. (2003). A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5, 367-377.
46. Vinson, C. R., Conover, S., and Adler, P. N. (1989). A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338, 263-264.
47. Wang, H. Y., Liu, T., and Malbon, C. C. (2006). Structure-function analysis of Frizzleds. Cell Signal. 18, 934-941.
48. Weeraratna, A. T., Jiang, Y., Hostetter, G., Rosenblatt, K., Duray, P., Bittner, M., and Trent, J. M. (2002). Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1, 279-288.
49. Wehrli, M., Dougan, S. T., Caldwell, K., O'Keefe, L., Schwartz, S., Vaizel-Ohayon, D., Schejter, E., Tomlinson, A., and DiNardo, S. (2000). arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407, 527-530.
50. Winklbauer, R., Medina, A., Swain, R. K., and Steinbeisser, H. (2001). Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature 413, 856-860.
51. Wong, H. C., Bourdelas, A., Krauss, A., Lee, H. J., Shao, Y., Wu, D., Mlodzik, M., Shi, D. L., and Zheng, J. (2003). Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled. Mol. Cell 12, 1251-1260.
52. Wu, J., Klein, T. J., and Mlodzik, M. (2004). Subcellular localization of frizzled receptors, mediated by their cytoplasmic tails, regulates signaling pathway specificity. PLoS Biol. 2, E158.
53. Yang-Snyder, J., Miller, J. R., Brown, J. D., Lai, C. J., and Moon, R. T. (1996). A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr. Biol. 6, 1302-1306.
54. Yao, R., Natsume, Y., and Noda, T. (2004). MAGI-3 is involved in the regulation of the JNK signaling pathway as a scaffold protein for frizzled and Ltap. Oncogene 23, 6023-6030.
55. Zimmermann, P., Meerschaert, K., Reekmans, G., Leenaerts, I., Small, J. V., Vandekerckhove, J., David, G., and Gettemans, J. (2002). PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol. Cell 9, 1215-1225.
56. Zimmermann, P., Tomatis, D., Rosas, M., Grootjans, J., Leenaerts, I., Degeest, G., Reekmans, G., Coomans, C., and David, G. (2001). Characterization of syntenin, a syndecan-binding PDZ protein, as a component of cell adhesion sites and microfilaments. Mol. Biol. Cell 12, 339-350.
57. Zimmermann, P., Zhang, Z., Degeest, G., Mortier, E., Leenaerts, I., Coomans, C., Schulz, J., N'Kuli, F., Courtoy, P. J., and David, G. (2005). Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell 9, 377-388.