Structural insights into the inhibition of Wnt signaling by cancer antigen 5T4/Wnt-activated inhibitory factor 1

Structure

Volumn 22, Issue 4, 2014, Pages 612-620

  Zhao, Yuguang ^a   Malinauskas, Tomas ^a,b   Harlos, Karl ^a   Jones, E Yvonne ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GLYCAN; LEUCINE; LEUCINE RICH REPEAT 1; TUMOR ANTIGEN; UNCLASSIFIED DRUG; WNT ACTIVATED INHIBITORY FACTOR 1; WNT PROTEIN; CANCER ANTIGEN 5T4; CELL SURFACE PROTEIN; LEUCINE-RICH REPEAT PROTEINS; MEMBRANE PROTEIN; PROTEIN; PROTEIN BINDING; TROPHOBLASTIC GLYCOPROTEIN 5T4, HUMAN;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; GLYCOSYLATION; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; AFFINITY CHROMATOGRAPHY; CELL MEMBRANE; CELL SURFACE; DISULFIDE BOND; FLUORESCENCE MICROSCOPY; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BETA CATENIN; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; WNT SIGNALING PATHWAY;

EID: 84898436061     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.01.009     Document Type: Article

References (45)

1. R.J. Amato, R.E. Hawkins, H.L. Kaufman, J.A. Thompson, P. Tomczak, C. Szczylik, M. McDonald, S. Eastty, W.H. Shingler, and J. de Belin et al. Vaccination of metastatic renal cancer patients with MVA-5T4: a randomized, double-blind, placebo-controlled phase III study Clin. Cancer Res. 16 2010 5539 5547
2. A.R. Aricescu, W. Lu, and E.Y. Jones A time- and cost-efficient system for high-level protein production in mammalian cells Acta Crystallogr. D Biol. Crystallogr. 62 2006 1243 1250
3. A. Awan, M.R. Lucic, D.M. Shaw, F. Sheppard, C. Westwater, S.A. Lyons, and P.L. Stern 5T4 interacts with TIP-2/GIPC, a PDZ protein, with implications for metastasis Biochem. Biophys. Res. Commun. 290 2002 1030 1036
4. E.R. Boghaert, L. Sridharan, K.M. Khandke, D. Armellino, M.G. Ryan, K. Myers, R. Harrop, A. Kunz, P.R. Hamann, and K. Marquette et al. The oncofetal protein, 5T4, is a suitable target for antibody-guided anti-cancer chemotherapy with calicheamicin Int. J. Oncol. 32 2008 221 234
5. E. Bourhis, W. Wang, C. Tam, J. Hwang, Y. Zhang, D. Spittler, O.W. Huang, Y. Gong, A. Estevez, and I. Zilberleyb et al. Wnt antagonists bind through a short peptide to the first β-propeller domain of LRP5/6 Structure 19 2011 1433 1442
6. R. Celikel, R.A. McClintock, J.R. Roberts, G.L. Mendolicchio, J. Ware, K.I. Varughese, and Z.M. Ruggeri Modulation of alpha-thrombin function by distinct interactions with platelet glycoprotein Ibalpha Science 301 2003 218 221
7. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
8. S. Chen, D. Bubeck, B.T. MacDonald, W.X. Liang, J.H. Mao, T. Malinauskas, O. Llorca, A.R. Aricescu, C. Siebold, X. He, and E.Y. Jones Structural and functional studies of LRP6 ectodomain reveal a platform for Wnt signaling Dev. Cell 21 2011 848 861
9. K. Cowtan Fitting molecular fragments into electron density Acta Crystallogr. D Biol. Crystallogr. 64 2008 83 89
10. R. DasGupta, A. Kaykas, R.T. Moon, and N. Perrimon Functional genomic analysis of the Wnt-wingless signaling pathway Science 308 2005 826 833
11. L. De Vries, X. Lou, G. Zhao, B. Zheng, and M.G. Farquhar GIPC, a PDZ domain containing protein, interacts specifically with the C terminus of RGS-GAIP Proc. Natl. Acad. Sci. USA 95 1998 12340 12345
12. P.R. Evans, and G.N. Murshudov How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69 2013 1204 1214
13. J.P. Gallivan, and D.A. Dougherty Cation-pi interactions in structural biology Proc. Natl. Acad. Sci. USA 96 1999 9459 9464
14. F. Glaser, T. Pupko, I. Paz, R.E. Bell, D. Bechor-Shental, E. Martz, and N. Ben-Tal ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information Bioinformatics 19 2003 163 164
15. R.S. Hodges, R.J. Heaton, J.M. Parker, L. Molday, and R.S. Molday Antigen-antibody interaction. Synthetic peptides define linear antigenic determinants recognized by monoclonal antibodies directed to the cytoplasmic carboxyl terminus of rhodopsin J. Biol. Chem. 263 1988 11768 11775
16. N. Hole, and P.L. Stern A 72 kD trophoblast glycoprotein defined by a monoclonal antibody Br. J. Cancer 57 1988 239 246
17. E.G. Huizinga, S. Tsuji, R.A. Romijn, M.E. Schiphorst, P.G. de Groot, J.J. Sixma, and P. Gros Structures of glycoprotein Ibalpha and its complex with von Willebrand factor A1 domain Science 297 2002 1176 1179
18. C.Y. Janda, D. Waghray, A.M. Levin, C. Thomas, and K.C. Garcia Structural basis of Wnt recognition by Frizzled Science 337 2012 59 64
19. W. Kabsch XDS Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
20. B. Kagermeier-Schenk, D. Wehner, G. Ozhan-Kizil, H. Yamamoto, J. Li, K. Kirchner, C. Hoffmann, P. Stern, A. Kikuchi, A. Schambony, and G. Weidinger Waif1/5T4 inhibits Wnt/β-catenin signaling and activates noncanonical Wnt pathways by modifying LRP6 subcellular localization Dev. Cell 21 2011 1129 1143
21. D.W. Kim, V. Krishnamurthy, S.D. Bines, and H.L. Kaufman TroVax, a recombinant modified vaccinia Ankara virus encoding 5T4: lessons learned and future development Hum. Vaccin. 6 2010 784 791
22. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D Biol. Crystallogr. 60 2004 2256 2268
23. B.T. MacDonald, K. Tamai, and X. He Wnt/β-catenin signaling: components, mechanisms, and diseases Dev. Cell 17 2009 9 26
24. T. Malinauskas Docking of fatty acids into the WIF domain of the human Wnt inhibitory factor-1 Lipids 43 2008 227 230
25. T. Malinauskas, A.R. Aricescu, W. Lu, C. Siebold, and E.Y. Jones Modular mechanism of Wnt signaling inhibition by Wnt inhibitory factor 1 Nat. Struct. Mol. Biol. 18 2011 886 893
26. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
27. R.S. Molday, and D. MacKenzie Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes Biochemistry 22 1983 653 660
28. I.S. Moreira, P.A. Fernandes, and M.J. Ramos Hot spots - a review of the protein-protein interface determinant amino-acid residues Proteins 68 2007 803 812
29. K. Mulryan, M.G. Ryan, K.A. Myers, D. Shaw, W. Wang, S.M. Kingsman, P.L. Stern, and M.W. Carroll Attenuated recombinant vaccinia virus expressing oncofetal antigen (tumor-associated antigen) 5T4 induces active therapy of established tumors Mol. Cancer Ther. 1 2002 1129 1137
30. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
31. K.A. Myers, V. Rahi-Saund, M.D. Davison, J.A. Young, A.J. Cheater, and P.L. Stern Isolation of a cDNA encoding 5T4 oncofetal trophoblast glycoprotein. An antigen associated with metastasis contains leucine-rich repeats J. Biol. Chem. 269 1994 9319 9324
32. T. Nagai, K. Ibata, E.S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications Nat. Biotechnol. 20 2002 87 90
33. K. Ohta, A. Ito, S. Kuriyama, G. Lupo, M. Kosaka, S. Ohnuma, S. Nakagawa, and H. Tanaka Tsukushi functions as a Wnt signaling inhibitor by competing with Wnt2b for binding to transmembrane protein Frizzled4 Proc. Natl. Acad. Sci. USA 108 2011 14962 14967
34. P. Polakis Drugging Wnt signalling in cancer EMBO J. 31 2012 2737 2746
35. P.J. Reeves, N. Callewaert, R. Contreras, and H.G. Khorana Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N- acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line Proc. Natl. Acad. Sci. USA 99 2002 13419 13424
36. P. Sapra, M. Damelin, J. Dijoseph, K. Marquette, K.G. Geles, J. Golas, M. Dougher, B. Narayanan, A. Giannakou, and K. Khandke et al. Long-term tumor regression induced by an antibody-drug conjugate that targets 5T4, an oncofetal antigen expressed on tumor-initiating cells Mol. Cancer Ther. 12 2013 38 47
37. E. Seiradake, C.H. Coles, P.V. Perestenko, K. Harlos, R.A. McIlhinney, A.R. Aricescu, and E.Y. Jones Structural basis for cell surface patterning through NetrinG-NGL interactions EMBO J. 30 2011 4479 4488
38. C. Söllner, and G.J. Wright A cell surface interaction network of neural leucine-rich repeat receptors Genome Biol. 10 2009 R99
39. P.J. Southall, G.M. Boxer, K.D. Bagshawe, N. Hole, M. Bromley, and P.L. Stern Immunohistological distribution of 5T4 antigen in normal and malignant tissues Br. J. Cancer 61 1990 89 95
40. T. Starzynska, P.J. Marsh, P.F. Schofield, S.A. Roberts, K.A. Myers, and P.L. Stern Prognostic significance of 5T4 oncofetal antigen expression in colorectal carcinoma Br. J. Cancer 69 1994 899 902
41. T.C. Terwilliger, R.W. Grosse-Kunstleve, P.V. Afonine, N.W. Moriarty, P.H. Zwart, L.W. Hung, R.J. Read, and P.D. Adams Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Acta Crystallogr. D Biol. Crystallogr. 64 2008 61 69
42. E.S. Trombetta, and A.J. Parodi Quality control and protein folding in the secretory pathway Annu. Rev. Cell Dev. Biol. 19 2003 649 676
43. T.S. Walter, J.M. Diprose, C.J. Mayo, C. Siebold, M.G. Pickford, L. Carter, G.C. Sutton, N.S. Berrow, J. Brown, and I.M. Berry et al. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization Acta Crystallogr. D Biol. Crystallogr. 61 2005 651 657
44. A.M. Woods, W.W. Wang, D.M. Shaw, C.M. Ward, M.W. Carroll, B.R. Rees, and P.L. Stern Characterization of the murine 5T4 oncofoetal antigen: a target for immunotherapy in cancer Biochem. J. 366 2002 353 365
45. Y. Zhao, B. Bishop, J.E. Clay, W. Lu, M. Jones, S. Daenke, C. Siebold, D.I. Stuart, E.Y. Jones, and A.R. Aricescu Automation of large scale transient protein expression in mammalian cells J. Struct. Biol. 175 2011 209 215