Frizzled-4 C-terminus distal to KTXXXW motif is essential for normal dishevelled recruitment and norrin-stimulated activation of Lef/Tcf-dependent transcriptional activation

Journal of Molecular Signaling

Volumn 11, Issue 1, 2016, Pages 1-7

  Bertalovitz, Alexander C ^a   Pau, Milly S ^a   Gao, Shujuan ^a   Malbon, Craig C ^a   Wang, Hsien Yu ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Carboxy terminus; Dishevelled; Frizzled; Frizzled 4; Helix VIII; Norrin

Indexed keywords

DISHEVELLED PROTEIN; FRIZZLED PROTEIN; G PROTEIN COUPLED RECEPTOR; LYMPHOID ENHANCER FACTOR 1; T CELL FACTOR PROTEIN;

ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; DNA SEQUENCE; ENZYME ACTIVITY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; LUCIFERASE ASSAY; PLASMID; POLYMERASE CHAIN REACTION; POST HOC ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION;

EID: 85007422254     PISSN: None     EISSN: 17502187     Source Type: Journal    
DOI: 10.5334/1750-2187-11-1     Document Type: Article

References (25)

1. Drake, MT, Shenoy, SK and Lefkowitz, RJ. Trafficking of G protein-coupled receptors. Circ Res. 2006; 99(6): 570-582. DOI: http://dx.doi.org/10.1161/01.RES.0000242563.47507.ce
2. Bockaert, J, Marin, P, Dumuis, A and Fagni, L. The 'magic tail' of G protein-coupled receptors: an anchorage for functional protein networks. FEBS Lett. 2003; 546(1): 65-72. Available at http://www.ncbi.nlm.nih.gov/pubmed/12829238. DOI: http://dx.doi.org/10.1016/S0014-5793(03)00453-8
3. Nie, J and Lewis, DL. The proximal and distal C-terminal tail domains of the CB1 cannabinoid receptor mediate G protein coupling. Neuroscience. 2001; 107(1): 161-167. Available at http://www.ncbi.nlm.nih.gov/pubmed/11744255. DOI: http://dx.doi.org/10.1016/S0306-4522(01)00335-9
4. Ahn, KH, Nishiyama, A, Mierke, DF and Kendall, DA. Hydrophobic residues in helix 8 of cannabinoid receptor 1 are critical for structural and functional properties. Biochemistry. 2010; 49(3): 502-511. DOI: http://dx.doi.org/10.1021/bi901619r
5. Swift, S, Leger, AJ, Talavera, J, Zhang, L, Bohm, A, et al. Role of the PAR1 receptor 8th helix in signaling: the 7-8-1 receptor activation mechanism. J Biol Chem. 2006; 281(7): 4109-4116. DOI: http://dx.doi.org/10.1074/jbc.M509525200
6. Wang, C, Wu, H, Katritch, V, Han, GW, Huang, XP, et al. Structure of the human smoothened receptor bound to an antitumour agent. Nature. 2013; 497(7449): 338-343. DOI: http://dx.doi.org/10.1038/nature12167
7. Rasmussen, SG, Choi, HJ, Rosenbaum, DM, Kobilka, TS, Thian, FS, et al. Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature. 2007; 450(7168): 383-387. DOI: http://dx.doi.org/10.1038/nature06325
8. Murakami, M and Kouyama, T. Crystal structure of squid rhodopsin. Nature. 2008; 453(7193): 363-367. DOI: http://dx.doi.org/10.1038/nature06925
9. Punchihewa, C, Ferreira, AM, Cassell, R, Rodrigues, P and Fujii, N. Sequence requirement and subtype specificity in the high-affinity interaction between human frizzled and dishevelled proteins. Protein Sci. 2009; 18(5): 994-1002. DOI: http://dx.doi.org/10.1002/pro.109
10. Lemma, V, D'Agostino, M, Caporaso, MG, Mallardo, M, Oliviero, G, et al. A disorder-toorder structural transition in the COOH-tail of Fz4 determines misfolding of the L501fsX533-Fz4 mutant. Sci Rep. 2013; 3: 2659. DOI: http://dx.doi.org/10.1038/srep02659
11. Umbhauer, M, Djiane, A, Goisset, C, Penzo-Mendez, A, Riou, JF, et al. The C-terminal cytoplasmic Lys-thr-X-X-X-Trp motif in frizzled receptors mediates Wnt/beta-catenin signalling. EMBO J. 2000; 19(18): 4944-4954. DOI: http://dx.doi.org/10.1093/emboj/19.18.4944
12. Schweizer, L and Varmus, H. Wnt/Wingless signaling through beta-catenin requires the function of both LRP/Arrow and frizzled classes of receptors. BMC Cell Biol. 2003; 4: 4. DOI: http://dx.doi.org/10.1186/1471-2121-4-4
13. Yu, H, Ye, X, Guo, N and Nathans, J. Frizzled 2 and frizzled 7 function redundantly in convergent extension and closure of the ventricular septum and palate: evidence for a network of interacting genes. Development. 2012; 139(23): 4383-4394. DOI: http://dx.doi.org/10.1242/dev.083352
14. Atwood, BK, Lopez, J, Wager-Miller, J, Mackie, K and Straiker, A. Expression of G protein-coupled receptors and related proteins in HEK293, AtT20, BV2, and N18 cell lines as revealed by microarray analysis. BMC Genomics. 2011; 12: 14. DOI: http://dx.doi.org/10.1186/1471-2164-12-14
15. Xu, Q, Wang, YS, Dabdoub, A, Smallwood, PM, Williams, J, et al. Vascular development in the retina and inner ear: Control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell. 2004; 116(6): 883-895. DOI: http://dx.doi.org/10.1016/S0092-8674(04)00216-8
16. Smallwood, PM, Williams, J, Xu, Q, Leahy, DJ and Nathans, J. Mutational analysis of Norrin-Frizzled4 recognition. Journal of Biological Chemistry. 2007; 282(6): 4057-4068. DOI: http://dx.doi.org/10.1074/jbc.M609618200
17. Lee, YN, Gao, Y and Wang, HY. Differential mediation of the Wnt canonical pathway by mammalian Dishevelleds-1,-2, and-3. Cell Signal. 2008; 20(2): 443-452. DOI: http://dx.doi.org/10.1016/j.cellsig.2007.11.005
18. Cong, F, Schweizer, L and Varmus, H. Wnt signals across the plasma membrane to activate the beta-catenin pathway by forming oligomers containing its receptors, Frizzled and LRP. Development. 2004; 131(20): 5103-5115. DOI: http://dx.doi.org/10.1242/dev.01318
19. Lu, D, Zhao, Y, Tawatao, R, Cottam, HB, Sen, M, et al. Activation of the Wnt signaling pathway in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 2004; 101(9): 3118-3123. DOI: http://dx.doi.org/10.1073/pnas.0308648100
20. Binnerts, ME, Kim, KA, Bright, JM, Patel, SM, Tran, K, et al. R-Spondin1 regulates Wnt signaling by inhibiting internalization of LRP6. Proc Natl Acad Sci U S A. 2007; 104(37): 14700-14705. DOI: http://dx.doi.org/10.1073/pnas.0702305104
21. Gayen, S, Li, Q, Kim, YM and Kang, C. Structure of the C-terminal region of the Frizzled receptor 1 in detergent micelles. Molecules. 2013; 18(7): 8579-8590. DOI: http://dx.doi.org/10.3390/molecules18078579
22. Zezula, J and Freissmuth, M. The A(2A)-adenosine receptor: a GPCR with unique features? Br J Pharmacol. 2008; 153(Suppl 1): S184-190. DOI: http://dx.doi.org/10.1038/sj.bjp.0707674
23. Sensoy, O and Weinstein, H. A mechanistic role of Helix 8 in GPCRs: Computational modeling of the dopamine D2 receptor interaction with the GIPC1-PDZ-domain. Biochim Biophys Acta. 2015; 1848(4): 976-983. DOI: http://dx.doi.org/10.1016/j.bbamem.2014.12.002
24. Tauriello, DV, Jordens, I, Kirchner, K, Slootstra, JW, Kruitwagen, T, et al. Wnt/beta-catenin signaling requires interaction of the Dishevelled DEP domain and C terminus with a discontinuous motif in Frizzled. Proc Natl Acad Sci U S A. 2012; 109(14): E812-820. DOI: http://dx.doi.org/10.1073/pnas.1114802109
25. Kolben, T, Perobner, I, Fernsebner, K, Lechner, F, Geissler, C, et al. Dissecting the impact of Frizzled receptors in Wnt/beta-catenin signaling of human mesenchymal stem cells. Biol Chem. 2012; 393(12): 1433-1447 DOI: http://dx.doi.org/10.1515/hsz-2012-0186