Crystal structure of a β-catenin/APC complex reveals a critical role for APC phosphorylation in APC function

Molecular Cell

Volumn 15, Issue 4, 2004, Pages 523-533

  Xing, Yi ^a   Clements, Wilson K ^a   Le Trong, Isolde ^a   Hinds, Thomas R ^b   Stenkamp, Ronald ^a   Kimelman, David ^a   Xu, Wenqing ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN; REPETITIVE DNA; T CELL FACTOR PROTEIN;

ARTICLE; CHEMICAL ANALYSIS; CRYSTAL STRUCTURE; DNA FLANKING REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; AMINO ACID SEQUENCE; BETA CATENIN; CRYSTALLOGRAPHY, X-RAY; CYTOSKELETAL PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, NUCLEIC ACID; SEQUENCE ALIGNMENT; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ARMADILLO;

EID: 4344684495     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2004.08.001     Document Type: Article

References (50)

1. Aberle H., Bauer A., Stappert J., Kispert A., Kemler R. β-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16:1997;3797-3804
2. Behrens J., Jerchow B.A., Wurtele M., Grimm J., Asbrand C., Wirtz R., Kuhl M., Wedlich D., Birchmeier W. Functional interaction of an axin homolog, conductin, with β-catenin, APC, and GSK3β Science. 280:1998;596-599
3. Bhattacharya G., Boman B.M. Phosphorylation of the adenomatous polyposis coli protein and its possible regulatory effects in cells. Biochem. Biophys. Res. Commun. 208:1995;103-110
4. Bienz M. The subcellular destinations of APC proteins. Nat. Rev. Mol. Cell Biol. 3:2002;328-338
5. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54:1998;905-921
6. Easwaran V., Song V., Polakis P., Byers S. The ubiquitin-proteasome pathway and serine kinase activity modulate adenomatous polyposis coli protein-mediated regulation of β-catenin- lymphocyte enhancer-binding factor signaling. J. Biol. Chem. 274:1999;16641-16645
7. Farr G.H. 3rd, Ferkey D.M., Yost C., Pierce S.B., Weaver C., Kimelman D. Interaction among GSK-3, GBP, axin, and APC in Xenopus axis specification. J. Cell Biol. 148:2000;691-702
8. Fasolini M., Wu X., Flocco M., Trosset J.Y., Oppermann U., Knapp S. Hot spots in Tcf4 for the interaction with β-catenin. J. Biol. Chem. 278:2003;21092-21098
9. Graham T.A., Weaver C., Mao F., Kimelman D., Xu W. Crystal structure of a β-catenin/Tcf complex. Cell. 103:2000;885-896
10. Graham T.A., Ferkey D.M., Mao F., Kimelman D., Xu W. Tcf4 can specifically recognize β-catenin using alternative conformations. Nat. Struct. Biol. 8:2001;1048-1052
11. Graham T.A., Clements W.K., Kimelman D., Xu W. The crystal structure of the β-catenin/ICAT complex reveals the inhibitory mechanism of ICAT. Mol. Cell. 10:2002;563-571
12. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer. an environment for comparative protein modeling Electrophoresis. 18:1997;2714-2723
13. Hart M.J., de los Santos R., Albert I.N., Rubinfeld B., Polakis P. Downregulation of β-catenin by human Axin and its association with the APC tumor suppressor, β-catenin and GSK3 beta. Curr. Biol. 8:1998;573-581
14. Henderson B.R. Nuclear-cytoplasmic shuttling of APC regulates β-catenin subcellular localization and turnover. Nat. Cell Biol. 2:2000;653-660
15. Henderson B.R., Fagotto F. The ins and outs of APC and β-catenin nuclear transport. EMBO Rep. 3:2002;834-839
16. Hsu W., Zeng L., Costantini F. Identification of a domain of Axin that binds to the serine/threonine protein phosphatase 2A and a self-binding domain. J. Biol. Chem. 274:1999;3439-3445
17. Huber A.H., Weis W.I. The structure of the β-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin. Cell. 105:2001;391-402
18. Hulsken J., Birchmeier W., Behrens J. E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton. J. Cell Biol. 127:1994;2061-2069
19. Ikeda S., Kishida M., Matsuura Y., Usui H., Kikuchi A. GSK-3beta-dependent phosphorylation of adenomatous polyposis coli gene product can be modulated by β-catenin and protein phosphatase 2A complexed with Axin. Oncogene. 19:2000;537-545
20. Kinzler K.W., Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 87:1996;159-170
21. Kraulis P.J. Molscript. a program to produce both detailed and schematic plots of protein structure J. Appl. Crystallogr. 24:1991;946-950
22. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. Procheck. a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26:1993;283-291
23. Lee, E., Salic, A., Kruger, R., Heinrich, R., and Kirschner, M.W. (2003). The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PloS Biol. 1(1).
24. Li X., Yost H.J., Virshup D.M., Seeling J.M. Protein phosphatase 2A and its B56 regulatory subunit inhibit Wnt signaling in Xenopus. EMBO J. 20:2001;4122-4131
25. McRee D.E. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125:1999;156-165
26. Merritt E.A., Murphy M.E.P. RASTER3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D. 50:1994;869-873
27. Munemitsu S., Albert I., Souza B., Rubinfeld B., Polakis P. Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. USA. 92:1995;3046-3050
28. Navaza J. AMoRe. an automated package for molecular replacement Acta Crystallogr. A. 50:1994;157-163
29. Nicholls A., Sharp K.A., Honig B. Protein folding and association. insights from the interfacial and thermodynamic properties of hydrocarbons Proteins. 11:1991;281-296
30. Omer C.A., Miller P.J., Diehl R.E., Kral A.M. Identification of Tcf4 residues involved in high-affinity β-catenin binding. Biochem. Biophys. Res. Commun. 256:1999;584-590
31. Orford K., Crockett C., Jensen J.P., Weissman A.M., Byers S.W. Serine phosphorylation-regulated ubiquitination and degradation of β-catenin. J. Biol. Chem. 272:1997;24735-24738
32. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode, Vol. 276 (New York: Academic Press).
33. Peifer M., Polakis P. Wnt signaling in oncogenesis and embryogenesis-a look outside the nucleus. Science. 287:2000;1606-1609
34. Polakis P. The adenomatous polyposis coli (APC) tumor suppressor. Biochim. Biophys. Acta. 1332:1997;F127-F147
35. Polakis P. Casein kinase 1. a Wnt'er of disconnect Curr. Biol. 12:2002;R499-R501
36. Poy F., Lepourcelet M., Shivdasani R.A., Eck M.J. Structure of a human Tcf4-β-catenin complex. Nat. Struct. Biol. 8:2001;1053-1057
37. Ratcliffe M.J., Itoh K., Sokol S.Y. A positive role for the PP2A catalytic subunit in Wnt signal transduction. J. Biol. Chem. 275:2000;35680-35683
38. Rosin-Arbesfeld R., Townsley F., Bienz M. The APC tumour suppressor has a nuclear export function. Nature. 406:2000;1009-1012
39. Rubinfeld B., Souza B., Albert I., Muller O., Chamberlain S.H., Masiarz F.R., Munemitsu S., Polakis P. Association of the APC gene product with β-catenin. Science. 262:1993;1731-1734
40. Rubinfeld B., Albert I., Porfiri E., Fiol C., Munemitsu S., Polakis P. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science. 272:1996;1023-1026
41. Rubinfeld B., Tice D.A., Polakis P. Axin-dependent phosphorylation of the adenomatous polyposis coli protein mediated by casein kinase 1ε J. Biol. Chem. 276:2001;39037-39045
42. Seeling J.M., Miller J.R., Gil R., Moon R.T., White R., Virshup D.M. Regulation of β-catenin signaling by the B56 subunit of protein phosphatase 2A. Science. 283:1999;2089-2091
43. Spink E.K., Fridman S.G., Weis W.I. Molecular mechanisms of β-catenin recognition by adenomatous polyposis coli revealed by the structure of an APC-β-catenin complex. EMBO J. 20:2001;6203-6212
44. Su L.K., Vogelstein B., Kinzler K.W. Association of the APC tumor suppressor protein with catenins. Science. 262:1993;1734-1737
45. Tickenbrock L., Kossmeier K., Rehmann H., Herrmann C., Muller O. Differences between the interaction of β-catenin with non-phosphorylated and single-mimicked phosphorylated 20-amino acid residue repeats of the APC protein. J. Mol. Biol. 327:2003;359-367
46. van de Wetering M., Cavallo R., Dooijes D., van Beest M., van Es J., Loureiro J., Ypma A., Hursh D., Jones T., Bejsovec A., et al. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell. 88:1997;789-799
47. van Es J.H., Kirkpatrick C., van de Wetering M., Molenaar M., Miles A., Kuipers J., Destree O., Peifer M., Clevers H. Identification of APC2, a homologue of the adenomatous polyposis coli tumour suppressor. Curr. Biol. 9:1999;105-108
48. von Kries J.P., Winbeck G., Asbrand C., Schwarz-Romond T., Sochnikova N., Dell'Oro A., Behrens J., Birchmeier W. Hot spots in β-catenin for interactions with LEF-1, conductin and APC. Nat. Struct. Biol. 7:2000;800-807
49. Xing Y., Clements W.K., Kimelman D., Xu W. Crystal structure of a β-catenin/axin complex suggests a mechanism for the β-catenin destruction complex. Genes Dev. 17:2003;2753-2764
50. Yamamoto H., Hinoi T., Michiue T., Fukui A., Usui H., Janssens V., Van Hoof C., Goris J., Asashima M., Kikuchi A. Inhibition of the Wnt signaling pathway by the PR61 subunit of protein phosphatase 2A. J. Biol. Chem. 276:2001;26875-26882