ADP-ribosylation factors 1 and 6 regulate Wnt/β-catenin signaling via control of LRP6 phosphorylation

Oncogene

Volumn 32, Issue 28, 2013, Pages 3390-3396

  Kim, W ^a   Kim, S Y ^b   Kim, T ^a   Kim, M ^a   Bae, D J ^a   Choi, H I ^b   Kim, I S ^b,c   Jho, E ^a  

^a University of Seoul   (South Korea)

^b Kyungpook National University   (South Korea)

^c Korea Institute of Science and Technology   (South Korea)

Author keywords

ADP ribosylation factor (Arf); LRP6; Phosphatidylinositol 4,5 bisphosphate (PtdIns (4,5)P2); Signal transduction; Wnt

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 2; BETA CATENIN; FRIZZLED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; WNT PROTEIN;

ARTICLE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTORS; ANIMALS; BETA CATENIN; FRIZZLED RECEPTORS; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MICE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME FACTORS; WNT3A PROTEIN;

EID: 84880281030     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.373     Document Type: Article

References (40)

1. MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 2009; 17: 9-26.
2. Davidson G, Wu W, Shen J, Bilic J, Fenger U, Stannek P et al. Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 2005; 438: 867-872.
3. Tamai K, Zeng X, Liu C, Zhang X, Harada Y, Chang Z et al. A mechanism for Wnt coreceptor activation. Mol Cell 2004; 13: 149-156.
4. Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R et al. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 2005; 438: 873-877.
5. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127: 469-480.
6. He X, Semenov M, Tamai K, Zeng XLDL. receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way. Development 2004; 131: 1663-1677.
7. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004; 20: 781-810.
8. Zhang Q, Major MB, Takanashi S, Camp ND, Nishiya N, Peters EC et al. Smallmolecule synergist of the Wnt/beta-catenin signaling pathway. Proc Natl Acad Sci USA 2007; 104: 7444-7448.
9. Santy LC, Casanova JE. Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J Cell Biol 2001; 154: 599-610.
10. Kahn RA, Cherfils J, Elias M, Lovering RC, Munro S, Schurmann A. Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins. J Cell Biol 2006; 172: 645-650.
11. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006; 7: 347-358.
12. Gillingham AK, Munro S. The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 2007; 23: 579-611.
13. Shin HW, Nakayama K. Guanine nucleotide-exchange factors for arf GTPases: their diverse functions in membrane traffic. J Biochem 2004; 136: 761-767.
14. Pan W, Choi SC, Wang H, Qin Y, Volpicelli-Daley L, Swan L et al. Wnt3a-mediated formation of phosphatidylinositol 4,5-bisphosphate regulates LRP6 phosphorylation. Science 2008; 321: 1350-1353.
15. Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C et al. ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat Cell Biol 1999; 1: 280-287.
16. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H et al. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 1999; 99: 521-532.
17. Giguere P, Rochdi MD, Laroche G, Dupre E, Whorton MR, Sunahara RK et al. ARF6 activation by Galpha q signaling: Galpha q forms molecular complexes with ARNO and ARF6. Cell Signal 2006; 18: 1988-1994.
18. Hall B, McLean MA, Davis K, Casanova JE, Sligar SG, Schwartz MA. A fluorescence resonance energy transfer activation sensor for Arf6. Anal Biochem 2008; 374: 243-249.
19. Jackson CL, Casanova JE. Turning on ARF: the Sec7 family of guanine-nucleotideexchange factors. Trends Cell Biol 2000; 10: 60-67.
20. MacDonald BT, Yokota C, Tamai K, Zeng X, He X. Wnt signal amplification via activity, cooperativity, and regulation of multiple intracellular PPPSP motifs in the Wnt co-receptor LRP6. J Biol Chem 2008; 283: 16115-16123.
21. Wong HC, Bourdelas A, Krauss A, Lee HJ, Shao Y, Wu D et al. Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled. Mol Cell 2003; 12: 1251-1260.
22. Hsieh JC, Rattner A, Smallwood PM, Nathans J. Biochemical characterization of Wnt-frizzled interactions using a soluble, biologically active vertebrate Wnt protein. Proc Natl Acad Sci USA 1999; 96: 3546-3551.
23. Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M et al. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 2007; 316: 1619-1622.
24. Perez-Mansilla B, Ha VL, Justin N, Wilkins AJ, Carpenter CL, Thomas GM. The differential regulation of phosphatidylinositol 4-phosphate 5-kinases and phospholipase D1 by ADP-ribosylation factors 1 and 6. Biochim Biophys Acta 2006; 1761: 1429-1442.
25. Nishioka T, Aoki K, Hikake K, Yoshizaki H, Kiyokawa E, Matsuda M. Rapid turnover rate of phosphoinositides at the front of migrating MDCK cells. Mol Biol Cell 2008; 19: 4213-4223.
26. Suzuki T, Kanai Y, Hara T, Sasaki J, Sasaki T, Kohara M et al. Crucial role of the small GTPase ARF6 in hepatic cord formation during liver development. Mol Cell Biol 2006; 26: 6149-6156.
27. Willert K, Shibamoto S, Nusse R. Wnt-induced dephosphorylation of axin releases beta-catenin from the axin complex. Genes Dev 1999; 13: 1768-1773.
28. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP et al. Wnt Signaling through Inhibition of beta-Catenin Degradation in an Intact Axin1 Complex. Cell 2012; 149: 1245-1256.
29. Liu X, Rubin JS, Kimmel AR. Rapid Wnt-induced changes in GSK3beta associations that regulate beta-catenin stabilization are mediated by Galpha proteins. Curr Biol 2005; 15: 1989-1997.
30. Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, Long F. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 2008; 133: 340-353.
31. Kumari S, Mayor S. ARF1 is directly involved in dynamin-independent endocytosis. Nat Cell Biol 2008; 10: 30-41.
32. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 2004; 15: 3542-3552.
33. Gagliardi M, Piddini E, Vincent JP. Endocytosis: a positive or a negative influence on Wnt signalling? Traffic 2008; 9: 1-9.
34. Yamamoto H, Komekado H, Kikuchi A. Caveolin is necessary for Wnt-3a-dependent internalization of LRP6 and accumulation of beta-catenin. Dev Cell 2006; 11: 213-223.
35. Sakane H, Yamamoto H, Kikuchi A. LRP6 is internalized by Dkk1 to suppress its phosphorylation in the lipid raft and is recycled for reuse. J Cell Sci 2010; 123(Pt 3): 360-368.
36. Nishida K, Yamasaki S, Hasegawa A, Iwamatsu A, Koseki H, Hirano T. Gab2 via PI- 3K, regulates ARF1 in FcepsilonRI-mediated granule translocation and mast cell degranulation. J Immunol 2011; 187: 932-941.
37. Sawano A, Miyawaki A. Directed evolution of green fluorescent protein by a new versatile PCR strategy for site-directed and semi-random mutagenesis. Nucleic Acids Res 2000; 28: E78.
38. Brummelkamp TR, Bernards R, Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002; 296: 550-553.
39. Tiscornia G, Singer O, Ikawa M, Verma IM. A general method for gene knockdown in mice by using lentiviral vectors expressing small interfering RNA. Proc Natl Acad Sci USA 2003; 100: 1844-1848.
40. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ et al. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 2006; 314: 1458-1461.