The tyrosine Y2502.39 in Frizzled 4 defines a conserved motif important for structural integrity of the receptor and recruitment of Disheveled

Cellular Signalling

Volumn 38, Issue , 2017, Pages 85-96

  Strakova, Katerina ^a,b   Matricon, Pierre ^c   Yokota, Chika ^b   Arthofer, Elisa ^d   Bernatik, Ondrej ^a   Rodriguez, David ^e   Arenas, Ernest ^b   Carlsson, Jens ^c   Bryja, Vitezslav ^a   Schulte, Gunnar ^a,b  

^a MASARYK UNIVERSITY   (Czech Republic)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Disheveled; DVL2; Frizzled; FZD4; GNA12; GNA13

Indexed keywords

BETA CATENIN; DISHEVELLED 2; FRIZZLED 4 PROTEIN; FRIZZLED PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; TYROSINE; UNCLASSIFIED DRUG; DISHEVELLED PROTEIN; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN BINDING;

ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOLECULAR MODEL; MUTATIONAL ANALYSIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; WNT SIGNALING PATHWAY; XENOPUS LAEVIS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CONSERVED SEQUENCE; DNA MUTATIONAL ANALYSIS; EMBRYOLOGY; HEK293 CELL LINE; METABOLISM; NEOPLASM; NONMAMMALIAN EMBRYO; PATHOLOGY; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; WNT SIGNALING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; DISHEVELLED PROTEINS; DNA MUTATIONAL ANALYSIS; EMBRYO, NONMAMMALIAN; FRIZZLED RECEPTORS; HEK293 CELLS; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; MOLECULAR DYNAMICS SIMULATION; NEOPLASMS; POLYMERIZATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; TYROSINE; WNT SIGNALING PATHWAY; XENOPUS LAEVIS;

EID: 85021746143     PISSN: 08986568     EISSN: 18733913     Source Type: Journal    
DOI: 10.1016/j.cellsig.2017.06.018     Document Type: Article

References (49)

1. Schulte, G., International union of basic and clinical pharmacology. LXXX. The class frizzled receptors. Pharmacol. Rev. 62 (2010), 632–667, 10.1124/pr.110.002931.632.
2. MacDonald, B.T., Semenov, M.V., He, X., SnapShot: Wnt/beta-catenin signaling. Cell 131 (2007), 36–37, 10.1016/j.cell.2007.11.036.
3. Gao, C., Chen, Y.-G., Dishevelled: the hub of Wnt signaling. Cell. Signal. 22 (2010), 717–727, 10.1016/j.cellsig.2009.11.021.
4. Schwarz-Romond, T., Fiedler, M., Shibata, N., Butler, P.J.G., Kikuchi, A., Higuchi, Y., Bienz, M., The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat. Struct. Mol. Biol. 14 (2007), 484–492, 10.1038/nsmb1247.
5. Bernatik, O., Sri Ganji, R., Dijksterhuis, J.P., Konik, P., Cervenka, I., Polonio, T., Krejci, P., Schulte, G., Bryja, V., Sequential activation and inactivation of dishevelled in the Wnt/beta-catenin pathway by casein kinases. J. Biol. Chem. 286 (2011), 10396–10410, 10.1074/jbc.M110.169870.
6. Axelrod, J.D., Miller, J.R., Shulman, J.M., Moon, R.T., Perrimon, N., Differential recruitment of dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12 (1998), 2610–2622, 10.1101/gad.12.16.2610.
7. Wong, H.-C., Bourdelas, A., Krauss, A., Lee, H.-J., Shao, Y., Wu, D., Mlodzik, M., Shi, D.-L., Zheng, J., Axelrod, J.D., Axelrod, J.D., Miller, J.R., Shulman, J.M., Moon, R.T., Perrimon, N., Bezprozvanny, I., Maximov, A., Boutros, M., Mlodzik, M., Boutros, M., Paricio, N., Strutt, D.I., Mlodzik, M., Cadigan, K.M., Nusse, R., Cheyette, B.N., Waxman, J.S., Miller, J.R., Takemaru, K., Sheldahl, L.C., Khlebtsova, N., Fox, E.P., Earnest, T., Moon, R.T., Cowburn, D., Daniels, D.L., Cohen, A.R., Anderson, J.M., Brunger, A.T., Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., Bax, A., Djiane, A., Riou, J.F., Umbhauer, M., Shi, D.L., Gloy, J., Hikasa, H., Sokol, S.Y., Guntert, P., Braun, W., Wuthrich, K., Guntert, P., Mumenthaler, C., Wuthrich, K., Hillier, B.J., Christopherson, K.S., Prehoda, K.E., Bredt, D.S., Lim, W.A., Hung, A.Y., Sheng, M., Krasnow, R.E., Wong, L.L., Adler, P.N., Li, L., Yuan, H., Xie, W., Mao, J., Caruso, A.M., McMahon, A., Sussman, D.J., Wu, D., Moon, R.T., Shah, K., Moon, R.T., Bowerman, B., Boutros, M., Perrimon, N., Noordermeer, J., Klingensmith, J., Perrimon, N., Nusse, R., Nooren, I.M., Thornton, J.M., Park, M., Moon, R.T., Rothbacher, U., Laurent, M.N., Deardorff, M.A., Klein, P.S., Cho, K.W., Fraser, S.E., Rousset, R., Mack, J.A., Wharton, K.A., Axelrod, J.D., Cadigan, K.M., Fish, M.P., Nusse, R., Scott, M.P., Shulman, J.M., Perrimon, N., Axelrod, J.D., Siegfried, E., Wilder, E.L., Perrimon, N., Sokol, S.Y., Taipale, J., Beachy, P.A., Tochio, H., Mok, Y.K., Zhang, Q., Kan, H.M., Bredt, D.S., Zhang, M., Tree, D.R., Shulman, J.M., Rousset, R., Scott, M.P., Gubb, D., Axelrod, J.D., Umbhauer, M., Djiane, A., Goisset, C., Penzo-Mendez, A., Riou, J.F., Boucaut, J.C., Shi, D.L., Weston, C.R., Davis, R.J., Wharton, K.A., Wong, H.C., Mao, J., Nguyen, J.T., Srinivas, S., Zhang, W., Liu, B., Li, L., Wu, D., Zheng, J., Wong, H.C., Liu, G., Zhang, Y.M., Rock, C.O., Zheng, J., Wuthrich, K., Xia, T.-H., Bartels, C., Wuthrich, K., Yan, D., Wallingford, J.B., Sun, T.Q., Nelson, A.M., Sakanaka, C., Reinhard, C., Harland, R.M., Fantl, W.J., Williams, L.T., Zheng, J., Cahill, S.M., Lemmon, M.A., Fushman, D., Schlessinger, J., Cowburn, D., Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled. Mol. Cell. 12 (2003), 1251–1260, 10.1016/s1097-2765(03)00427-1.
8. Cong, F., Schweizer, L., Varmus, H., Wnt signals across the plasma membrane to activate the beta-catenin pathway by forming oligomers containing its receptors, Frizzled and LRP. Development 131 (2004), 5103–5115, 10.1242/dev.01318.
9. Pau, M.S., Gao, S., Malbon, C.C., Wang, H., Bertalovitz, A.C., The intracellular loop 2 F328S frizzled-4 mutation implicated in familial exudative vitreoretinopathy impairs dishevelled recruitment. J. Mol. Signal. 10 (2015), 1–10, 10.5334/1750-2187-10-6.
10. Tauriello, D.V.F., Jordens, I., Kirchner, K., Slootstra, J.W., Kruitwagen, T., Bouwman, B.A.M., Noutsou, M., Rüdiger, S.G.D., Schwamborn, K., Schambony, A., Maurice, M.M., Wnt/β-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., 109, 2012, E812-20, 10.1073/pnas.1114802109.
11. Bertalovitz, A.C., Pau, M.S., Gao, S., Malbon, C.C., Wang, H., Frizzled-4 C-terminus distal to KTXXXW motif is essential for normal dishevelled recruitment and Norrin-stimulated activation of Lef/Tcf-dependent transcriptional activation. J. Mol. Signal. 11 (2016), 1–7, 10.5334/1750-2187-11-1.
12. Wong, H.C., Mao, J., Nguyen, J.T., Srinivas, S., Zhang, W., Liu, B., Li, L., Wu, D., Zheng, J., Structural basis of the recognition of the dishevelled DEP domain in the Wnt signaling pathway. Nat. Struct. Biol. 7 (2000), 1178–1184, 10.1038/82047.
13. Simons, M., Gault, W.J., Gotthardt, D., Rohatgi, R., Klein, T.J., Shao, Y., Lee, H.-J., Wu, A.-L., Fang, Y., Satlin, L.M., Dow, J.T., Chen, J., Zheng, J., Boutros, M., Mlodzik, M., Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization. Nat. Cell Biol. 11 (2009), 286–294, 10.1038/ncb1836.
14. Gammons, M.V., Renko, M., Johnson, C.M., Rutherford, T.J., Bienz, M., Wnt signalosome assembly by DEP domain swapping of dishevelled. Mol. Cell, 2016, 1–13, 10.1016/j.molcel.2016.08.026.
15. Arthofer, E., Hot, B., Petersen, J., Strakova, K., Jäger, S., Grundmann, M., Kostenis, E., Gutkind, J.S., Schulte, G., WNT stimulation dissociates a frizzled 4 inactive-state complex with Gα12/13. Mol. Pharmacol., 90, 2016, 10.1124/mol.116.104919.
16. Regard, J.B., Sato, I.T., Coughlin, S.R., Anatomical profiling of G protein-coupled receptor expression. Cell 135 (2008), 561–571, 10.1016/j.cell.2008.08.040.
17. Ye, X., Wang, Y., Cahill, H., Yu, M., Badea, T.C., Smallwood, P.M., Peachey, N.S., Nathans, J., Norrin, Frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization. Cell 139 (2009), 285–298, 10.1016/j.cell.2009.07.047.
18. Robitaille, J., MacDonald, M.L.E., Kaykas, A., Sheldahl, L.C., Zeisler, J., Dubé, M.-P., Zhang, L.-H., Singaraja, R.R., Guernsey, D.L., Zheng, B., Siebert, L.F., Hoskin-Mott, A., Trese, M.T., Pimstone, S.N., Shastry, B.S., Moon, R.T., Hayden, M.R., Goldberg, Y.P., Samuels, M.E., Mutant frizzled-4 disrupts retinal angiogenesis in familial exudative vitreoretinopathy. Nat. Genet. 32 (2002), 326–330, 10.1038/ng957.
19. Nieuwkoop, P., Faber, J., Normal Table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg Till the End of Metamorphosis. 1994, Garland Science.
20. Darras, S., Marikawa, Y., Elinson, R.P., Lemaire, P., Animal and vegetal pole cells of early Xenopus embryos respond differently to maternal dorsal determinants: implications for the patterning of the organiser. Development 124 (1997), 4275–4286.
21. Heasman, J., Kofron, M., Wylie, C., β-Catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev. Biol. 222 (2000), 124–134, 10.1006/dbio.2000.9720.
22. Hot, B., Valnohova, J., Arthofer, E., Simon, K., Shin, J., Uhlén, M., Kostenis, E., Mulder, J., Schulte, G., FZD 10-G α 13 signalling axis points to a role of FZD 10 in CNS angiogenesis. Cell. Signal. 32 (2017), 93–103, 10.1016/j.cellsig.2017.01.023.
23. Wang, C., Wu, H., Evron, T., Vardy, E., Han, G.W., Huang, X.-P., Hufeisen, S.J., Mangano, T.J., Urban, D.J., Katritch, V., Cherezov, V., Caron, M.G., Roth, B.L., Stevens, R.C., Structural basis for smoothened receptor modulation and chemoresistance to anticancer drugs. Nat. Commun., 5, 2014, 4355, 10.1038/ncomms5355.
24. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., Mcgettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., Clustal W and Clustal X version 2.0. Bioinformatics 23 (2007), 2947–2948, 10.1093/bioinformatics/btm404.
25. Webb, B., Sali, A., Comparative protein structure modeling using MODELLER. Curr. Protoc. Protein Sci., 2014, 10.1002/0471250953.bi0506s47.
26. Abraham, M.J., Murtola, T., Schulz, R., Páall, S., Smith, J.C., Hess, B., Lindah, E., Gromacs: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2 (2015), 19–25, 10.1016/j.softx.2015.06.001.
27. Rodríguez, D., Piñeiro, Á., Gutiérrez-De-Terán, H., Molecular dynamics simulations reveal insights into key structural elements of adenosine receptors. Biochemistry 50 (2011), 4194–4208, 10.1021/bi200100t.
28. Jorgensen, W.L., Maxwell, D.S., Tirado-Rives, J., Development and testing of the OLPS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118 (1996), 11225–11236, 10.1021/ja9621760.
29. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., Klein, M.L., Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 1983, 926, 10.1063/1.445869.
30. Hess, B., Bekker, H., Berendsen, H.J.C., Fraaije, J.G.E.M., LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18 (1997), 1463–1472, 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H.
31. Miyamoto, S., Kollman, P.A., Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 13 (1992), 952–962.
32. Chakrabarti, N., Neale, C., Payandeh, J., Pai, E.F., Pomès, R., An iris-like mechanism of pore dilation in the CorA magnesium transport system. Biophys. J. 98 (2010), 784–792, 10.1016/j.bpj.2009.11.009.
33. Lindahl, E., Edholm, O., Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations. Biophys. J. 79 (2000), 426–433, 10.1016/S0006-3495(00)76304-1.
34. Berger, O., Edholm, O., Jahnig, F., Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72 (1997), 2002–2013, 10.1016/S0006-3495(97)78845-3.
35. Darden, T., York, D., Pedersen, L., Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J. Chem. Phys., 98, 1993, 10089, 10.1063/1.464397.
36. Nosé, S., Klein, M.L., Constant pressure molecular dynamics for molecular systems. Mol. Phys. 50 (1983), 1055–1076.
37. Parrinello, M., Rahman, A., Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52 (1981), 7182–7190, 10.1063/1.328693.
38. Schindelin, J., Arganda-carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A., Fiji: an open-source platform for biological-image analysis. Nat. Methods, 9, 2012, 10.1038/nmeth.2019.
39. Vohra, S., Taddese, B., Conner, A.C., Poyner, D.R., Hay, D.L., Barwell, J., Reeves, P.J., Upton, G.J.G., Reynolds, C.A., Similarity between class A and class B G-protein-coupled receptors exemplified through calcitonin gene-related peptide receptor modelling and mutagenesis studies. J. R. Soc. Interface, 10, 2013, 20120846, 10.1098/rsif.2012.0846.
40. Wang, C., Wu, H., Katritch, V., Han, G.W., Huang, X.-P., Liu, W., Siu, F.Y., Roth, B.L., Cherezov, V., Stevens, R.C., Structure of the human smoothened receptor bound to an antitumour agent. Nature 497 (2013), 338–343, 10.1038/nature12167.
41. Bryja, V., Schulte, G., Rawal, N., Grahn, A., Arenas, E., Wnt-5a induces dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J. Cell Sci. 120 (2007), 586–595, 10.1242/jcs.03368.
42. Bryja, V., Gradl, D., Schambony, A., Arenas, E., Schulte, G., Beta-arrestin is a necessary component of Wnt/beta-catenin signaling in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 6690–6695, 10.1073/pnas.0611356104.
43. Bryja, V., Schambony, A., Cajánek, L., Dominguez, I., Arenas, E., Schulte, G., Beta-arrestin and casein kinase 1/2 define distinct branches of non-canonical WNT signalling pathways. EMBO Rep. 9 (2008), 1244–1250, 10.1038/embor.2008.193.
44. He, X., Saint-Jeannet, J.P., Wang, Y., Nathans, J., Dawid, I., Varmus, H., A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275 (1997), 1652–1654, 10.1126/science.275.5306.1652.
45. Djiane, A., Riou, J.-F.R., Umbhauer, M., Boucaut, J.-C., Shi, D.-L., Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 127 (2000), 3091–3100, 10.1242/dev.00435.
46. Park, H.W., Kim, Y.C., Yu, B., Alexander, C.M., Wang, C., Park, H.W., Kim, Y.C., Yu, B., Moroishi, T., Mo, J., Plouffe, S.W., Meng, Z., Alternative Wnt signaling activates YAP/TAZ. Cell, 2015, 780–794, 10.1016/j.cell.2015.07.013.
47. Wisler, J.W., Xiao, K., Thomsen, A.R.B., Lefkowitz, R.J., Recent developments in biased agonism. Curr. Opin. Cell Biol. 27 (2014), 18–24, 10.1016/j.ceb.2013.10.008.
48. Gao, J., Aksoy, B.A., Dogrusoz, U., Dresdner, G., Gross, B., Sumer, S.O., Sun, Y., Jacobsen, A., Sinha, R., Larsson, E., Cerami, E., Sander, C., Schultz, N., Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal., 6, 2013, pl1, 10.1126/scisignal.2004088.
49. Cerami, E., Gao, J., Dogrusoz, U., Gross, B.E., Sumer, S.O., Aksoy, B.A., Jacobsen, A., Byrne, C.J., Heuer, M.L., Larsson, E., Antipin, Y., Reva, B., Goldberg, A.P., Sander, C., Schultz, N., The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2 (2012), 401–404, 10.1158/2159-8290.CD-12-0095.