Β-Arrestin promotes wnt-induced low density lipoprotein receptor-related protein 6 (Lrp6) phosphorylation via increased membrane recruitment of amer1 protein

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 1128-1141

  Kříž, Vítězslav ^a,b   Pospíchalová, Vendula ^a   Mašek, Jan ^a,f   Kilander, Michaela Brita Christina ^d   Slavík, Josef ^e   Tanneberger, Kristina ^c   Schulte, Gunnar ^a,d   MacHala, Miroslav ^e   Kozubík, Alois ^a,b   Behrens, Juergen ^c   Bryja, Vítězslav ^a,b  

^a MASARYK UNIVERSITY   (Czech Republic)

^b INSTITUTE OF BIOPHYSICS   (Czech Republic)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d KAROLINSKA INSTITUTE   (Sweden)

^e VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^f INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ARRESTINS; CATENIN SIGNALING; LOW DENSITY LIPOPROTEINS; MEMBRANE DYNAMICS;

PHOSPHORYLATION;

PROTEINS;

BETA ARRESTIN; BETA CATENIN; BINDING PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN AMER1; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3A PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; ENZYME SYNTHESIS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

AMER1/WTX/FAM123B; DVL; LRP6 PHOSPHORYLATION; MEMBRANE LIPIDS; PHOSPHATIDYLINOSITOL KINASE; PHOSPHATIDYLINOSITOL PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL SIGNALING; WNT SIGNALING; Β-ARRESTIN; Β-CATENIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ARRESTINS; BLOTTING, WESTERN; CELL MEMBRANE; CELLS, CULTURED; EMBRYO, MAMMALIAN; FIBROBLASTS; HEK293 CELLS; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; RNA INTERFERENCE; TUMOR SUPPRESSOR PROTEINS; WNT3A PROTEIN;

EID: 84891959525     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.498444     Document Type: Article

References (44)

1. Clevers, H. (2006) Wnt/-catenin signaling in development and disease. Cell 127, 469-480
2. Logan, C. Y., and Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810
3. Schulte, G., and Bryja, V. (2007) The Frizzled family of unconventional G protein-coupled receptors. Trends Pharmacol. Sci. 28, 518-525
4. Bilic, J., Huang, Y. L., Davidson, G., Zimmermann, T., Cruciat, C. M., Bienz, M., and Niehrs, C. (2007) Wnt induces LRP6 signalosomes and promotes Dishevelled-dependent LRP6 phosphorylation. Science 316, 1619-1622
5. Zeng, X., Huang, H., Tamai, K., Zhang, X., Harada, Y., Yokota, C., Almeida, K., Wang, J., Doble, B., Woodgett, J., Wynshaw-Boris, A., Hsieh, J. C., and He, X. (2008) Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via Frizzled, Dishevelled, and Axin functions. Development 135, 367-375
6. Pan, W., Choi, S. C., Wang, H., Qin, Y., Volpicelli-Daley, L., Swan, L., Lucast, L., Khoo, C., Zhang, X., Li, L., Abrams, C. S., Sokol, S. Y., and Wu, D. (2008) Wnt3a-mediated formation of phosphatidylinositol 4,5-bisphosphate regulates LRP6 phosphorylation. Science 321, 1350-1353
7. Tanneberger, K., Pfister, A. S., Brauburger, K., Schneikert, J., Hadjihannas, M. V., Kriz, V., Schulte, G., Bryja, V., and Behrens, J. (2011) Amer1/WTX couples Wnt-induced formation of PtdIns(4,5)P2 to LRP6 phosphorylation. EMBO J. 30, 1433-1443
8. Tamai, K., Zeng, X., Liu, C., Zhang, X., Harada, Y., Chang, Z., and He, X. (2004) A mechanism for Wnt coreceptor activation. Mol. Cell 13, 149-156
9. Behrens, J., Jerchow, B. A., Würtele, M., Grimm, J., Asbrand, C., Wirtz, R., Kühl, M., Wedlich, D., and Birchmeier, W. (1998) Functional interaction of an Axin homolog, conductin, with-catenin, APC, and GSK3-. Science 280, 596-599
10. Kimelman, D., and Xu, W. (2006)-Catenin destruction complex: insights and questions from a structural perspective. Oncogene 25, 7482-7491
11. MacDonald, B. T., Tamai, K., and He, X. (2009) Wnt/-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26
12. Schulte, G., Schambony, A., and Bryja, V. (2010) Arrestins: scaffolds and signalling elements essential for WNT/Frizzled signalling pathways? Br. J. Pharmacol. 159, 1051-1058
13. Chen, W., Hu, L. A., Semenov, M. V., Yanagawa, S., Kikuchi, A., Lefkowitz, R. J., and Miller, W. E. (2001) Arrestin1 modulates lymphoid enhancer factor transcriptional activity through interaction with phosphorylated Dishevelled proteins. Proc. Natl. Acad. Sci. U.S.A. 98, 14889-14894
14. Bryja, V., Gradl, D., Schambony, A., Arenas, E., and Schulte, G. (2007) Arrestin is a necessary component of Wnt/-catenin signaling in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 6690-6695
15. Bryja, V., Schambony, A., Cajánek, L., Dominguez, I., Arenas, E., and Schulte, G. (2008) Arrestin and casein kinase 1/2 define distinct branches of noncanonical WNT signalling pathways. EMBO Rep. 9, 1244-1250
16. Chen, W., ten Berge, D., Brown, J., Ahn, S., Hu, L. A., Miller, W. E., Caron, M. G., Barak, L. S., Nusse, R., and Lefkowitz, R. J. (2003) Dishevelled 2 recruits-arrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4. Science 301, 1391-1394
17. Kim, G. H., Her, J. H., and Han, J. K. (2008) Ryk cooperates with Frizzled 7 to promote Wnt11-mediated endocytosis and is essential for Xenopus laevis convergent extension movements. J. Cell Biol. 182, 1073-1082
18. Kim, G. H., and Han, J. K. (2007) Essential role for-arrestin 2 in the regulation of Xenopus convergent extension movements. EMBO J. 26, 2513-2526
19. Kikuchi, A., Yamamoto, H., and Sato, A. (2009) Selective activation mechanisms of Wnt signaling pathways. Trends Cell Biol. 19, 119-129
20. Bernatik, O., Ganji, R. S., Dijksterhuis, J. P., Konik, P., Cervenka, I., Polonio, T., Krejci, P., Schulte, G., and Bryja, V. (2011) Sequential activation and inactivation of Dishevelled in the Wnt/-catenin pathway by casein kinases. J. Biol. Chem. 286, 10396-10410
21. Kohout, T. A., Lin, F. S., Perry, S. J., Conner, D. A., and Lefkowitz, R. J. (2001) Arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc. Natl. Acad. Sci. U.S.A. 98, 1601-1606
22. Tanneberger, K., Pfister, A. S., Kriz, V., Bryja, V., Schambony, A., and Behrens, J. (2011) Structural and functional characterization of the Wnt inhibitor APC membrane recruitment 1 (Amer1). J. Biol. Chem. 286, 19204-19214
23. Angers, S., Thorpe, C. J., Biechele, T. L., Goldenberg, S. J., Zheng, N., MacCoss, M. J., and Moon, R. T. (2006) The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-catenin pathway by targeting Dishevelled for degradation. Nat. Cell Biol. 8, 348-357
24. Tauriello, D. V., Haegebarth, A., Kuper, I., Edelmann, M. J., Henraat, M., Canninga-van Dijk, M. R., Kessler, B. M., Clevers, H., and Maurice, M. M. (2010) Loss of the tumor suppressor CYLD enhances Wnt/-catenin signaling through K63-linked ubiquitination of Dvl. Mol. Cell 37, 607-619
25. Lee, J. S., Ishimoto, A., and Yanagawa, S. (1999) Characterization of mouse Dishevelled (Dvl) proteins in Wnt/Wingless signaling pathway. J. Biol. Chem. 274, 21464-21470
26. Veeman, M. T., Slusarski, D. C., Kaykas, A., Louie, S. H., and Moon, R. T. (2003) Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13, 680-685
27. Grohmann, A., Tanneberger, K., Alzner, A., Schneikert, J., and Behrens, J. (2007) Amer1 regulates the distribution of the tumor suppressor APC between microtubules and the plasma membrane. J. Cell Sci. 120, 3738-3747
28. Bryja, V., Pacherník, J., Faldíková, L., Krejcí, P., Pogue, R., Nevrivá, I., Dvorák, P., and Hampl, A. (2004) The role of p27Kip1 in maintaining the levels of D-type cyclins in vivo. Biochim. Biophys. Acta 1691, 105-116
29. Major, M. B., Roberts, B. S., Berndt, J. D., Marine, S., Anastas, J., Chung, N., Ferrer, M., Yi, X., Stoick-Cooper, C. L., von Haller, P. D., Kategaya, L., Chien, A., Angers, S., MacCoss, M., Cleary, M. A., Arthur, W. T., and Moon, R. T. (2008) New regulators of Wnt/-catenin signaling revealed by integrative molecular screening. Sci. Signal. 1, ra12
30. Smalley, M. J., Signoret, N., Robertson, D., Tilley, A., Hann, A., Ewan, K., Ding, Y., Paterson, H., and Dale, T. C. (2005) Dishevelled (Dvl-2) activates canonical Wnt signalling in the absence of cytoplasmic puncta. J. Cell Sci. 118, 5279-5289
31. Schwarz-Romond, T., Merrifield, C., Nichols, B. J., and Bienz, M. (2005) The Wnt signalling effector Dishevelled forms dynamic protein assemblies rather than stable associations with cytoplasmic vesicles. J. Cell Sci. 118, 5269-5277
32. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K. W., Vogelstein, B., and Clevers, H. (1997) Constitutive transcriptional activation by a-catenin-TCF complex in APC-/-colon carcinoma. Science 275, 1784-1787
33. Qin, Y., Li, L., Pan, W., and Wu, D. (2009) Regulation of phosphatidylinositol kinases and metabolism by Wnt3a and Dvl. J. Biol. Chem. 284, 22544-22548
34. Nelson, C. D., Kovacs, J. J., Nobles, K. N., Whalen, E. J., and Lefkowitz, R. J. (2008) Arrestin scaffolding of phosphatidylinositol 4-phosphate 5-kinase I-promotes agonist-stimulated sequestration of the-2-adrenergic receptor. J. Biol. Chem. 283, 21093-21101
35. Balla, A., Tuymetova, G., Barshishat, M., Geiszt, M., and Balla, T. (2002) Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J. Biol. Chem. 277, 20041-20050
36. Major, M. B., Camp, N. D., Berndt, J. D., Yi, X., Goldenberg, S. J., Hubbert, C., Biechele, T. L., Gingras, A. C., Zheng, N., Maccoss, M. J., Angers, S., and Moon, R. T. (2007) Wilms tumor suppressor WTX negatively regulates WNT/-catenin signaling. Science 316, 1043-1046
37. Chen, M., Philipp, M., Wang, J., Premont, R. T., Garrison, T. R., Caron, M. G., Lefkowitz, R. J., and Chen, W. (2009) G protein-coupled receptor kinases phosphorylate LRP6 in the Wnt pathway. J. Biol. Chem. 284, 35040-35048
38. C? ervenka, I., Wolf, J., Mas?ek, J., Krejci, P., Wilcox, W. R., Kozubík, A., Schulte, G., Gutkind, J. S., and Bryja, V. (2011) Mitogen-activated protein kinases promote WNT/-catenin signaling via phosphorylation of LRP6. Mol. Cell. Biol. 31, 179-189
39. Krejci, P., Aklian, A., Kaucka, M., Sevcikova, E., Prochazkova, J., Masek, J. K., Mikolka, P., Pospisilova, T., Spoustova, T., Weis, M., Paznekas, W. A., Wolf, J. H., Gutkind, J. S., Wilcox, W. R., Kozubik, A., Jabs, E. W., Bryja, V., Salazar, L., Vesela, I., and Balek, L. (2012) Receptor tyrosine kinases activate canonical WNT/-catenin signaling via MAP kinase/LRP6 pathway and direct-catenin phosphorylation. PLoS ONE 7, e35826
40. Davidson, G., Wu, W., Shen, J., Bilic, J., Fenger, U., Stannek, P., Glinka, A., and Niehrs, C. (2005) Casein kinase 1-couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438, 867-872
41. Davidson, G., Shen, J., Huang, Y. L., Su, Y., Karaulanov, E., Bartscherer, K., Hassler, C., Stannek, P., Boutros, M., and Niehrs, C. (2009) Cell cycle control of Wnt receptor activation. Dev. Cell 17, 788-799
42. Zeng, X., Tamai, K., Doble, B., Li, S., Huang, H., Habas, R., Okamura, H., Woodgett, J., and He, X. (2005) A dual-kinase mechanism for Wnt coreceptor phosphorylation and activation. Nature 438, 873-877
43. Pfister, A. S., Tanneberger, K., Schambony, A., and Behrens, J. (2012) Amer2 protein is a novel negative regulator of Wnt/-catenin signaling involved in neuroectodermal patterning. J. Biol. Chem. 287, 1734-1741
44. Boutet, A., Comai, G., and Schedl, A. (2010) The WTX/Amer1 gene family: evolution, signature and function. BMC Evol. Biol. 10, 280