The two SAMP repeats and their phosphorylation state in Drosophila Adenomatous polyposis coli-2 play mechanistically distinct roles in negatively regulating Wnt signaling

Molecular Biology of the Cell

Volumn 26, Issue 24, 2015, Pages 4503-4518

  Kunttas Tatli, Ezgi ^a   Von Kleeck, Ryan A ^b   Greaves, Bradford D ^b   Vinson, David ^a   Roberts, David M ^b   McCartney, Brooke M ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b FRANKLIN AND MARSHALL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; BETA CATENIN; WNT PROTEIN; APC2 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; PROTEIN BINDING; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; BINDING AFFINITY; COLON POLYPOSIS; CONTROLLED STUDY; DROSOPHILA; EMBRYO; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SAMP REPEAT; WNT SIGNALING PATHWAY; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; COLORECTAL TUMOR; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; TRANSGENIC ANIMAL; TUMOR CELL LINE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXIN PROTEIN; BETA CATENIN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DROSOPHILA; DROSOPHILA PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR SUPPRESSOR PROTEINS; WNT SIGNALING PATHWAY;

EID: 84949034911     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-07-0515     Document Type: Article

References (43)

1. Ahmed Y, Nouri A, Wieschaus E (2002). Drosophila Apc1 and Apc2 regulate Wingless transduction throughout development. Development 129, 1751-1762.
2. Akong K, Grevengoed EE, Price MH, McCartney BM, Hayden MA, DeNofrio JC, Peifer M (2002). Drosophila APC2 and APC1 play overlapping roles in wingless signaling in the embryo and imaginal discs. Dev Biol 250, 91-100.
3. Behrens J, Jerchow BA, Würtele M, Grimm J, Asbrand C, Wirtz R, Kühl M, Wedlich D, Birchmeier W (1998). Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280, 596-599.
4. Beroud C (1996). APC gene: database of germline and somatic mutations in human tumors and cell lines. Nucleic Acids Res 24, 121-124.
5. Cadigan KM, Peifer M (2009). Wnt signaling from development to disease: insights from model systems. Cold Spring Harb Perspect Biol 1, a002881.
6. Chou TB, Perrimon N (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
7. Clevers H, Nusse R (2012). Wnt/β-catenin signaling and disease. Cell 149, 1192-1205.
8. Fagotto F, Jho EH, Zeng L, Kurth T, Joos T, Kaufmann C, Costantini F (1999). Domains of axin involved in protein-protein interactions, Wnt pathway inhibition, and intracellular localization. J Cell Biol 145, 741-756.
9. Faux MC, Coates JL, Catimel B, Cody S, Clayton AHA, Layton MJ, Burgess AW (2008). Recruitment of adenomatous polyposis coli and beta-catenin to axin-puncta. Oncogene 27, 5808-5820.
10. Fiedler M, Mendoza-Topaz C, Rutherford TJ, Mieszczanek J, Bienz M (2011). Dishevelled interacts with the DIX domain polymerization interface of Axin to interfere with its function in down-regulating β-catenin. Proc Natl Acad Sci USA 108, 1937-1942.
11. Ha N-C, Tonozuka T, Stamos JL, Choi H-J, Weis WI (2004). Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol Cell 15, 511-521.
12. Inestrosa NC, Varela-Nallar L (2014). Wnt signaling in the nervous system and in Alzheimer's disease. J Mol Cell Biol 6, 64-74.
13. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H (1997). Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/-colon carcinoma. Science 275, 1784-1787.
14. Kunttas-Tatli E, Roberts DM, McCartney BM (2014). Self-association of the APC tumor suppressor is required for the assembly, stability, and activity of the Wnt signaling destruction complex. Mol Biol Cell 25, 3424-3436.
15. Kunttas-Tatli E, Zhou M-N, Zimmerman S, Molinar O, Zhouzheng F, Carter K, Kapur M, Cheatle A, Decal R, McCartney BM (2012). Destruction complex function in the Wnt signaling pathway of Drosophila requires multiple interactions between Adenomatous polyposis coli 2 and Armadillo. Genetics 190, 1059-1075.
16. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach J P, Mohammed S, Heck AJ, Maurice MM, Mahmoudi T, Clevers H (2012). Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 149, 1245-1256.
17. Liu J, Xing Y, Hinds TR, Zheng J, Xu W (2006). The third 20 amino acid repeat is the tightest binding site of APC for beta-catenin. J Mol Biol 360, 133-144.
18. Marin O, Bustos VH, Cesaro L, Meggio F, Pagano MA, Antonelli M, Allende CC, Pinna LA, Allende JE (2003). A noncanonical sequence phosphorylated by casein kinase 1 in beta-catenin may play a role in casein kinase 1 targeting of important signaling proteins. Proc Natl Acad Sci USA 100, 10193-10200.
19. McCartney BM, Dierick HA, Kirkpatrick C, Moline MM, Baas A, Peifer M, Bejsovec A (1999). Drosophila APC2 is a cytoskeletally-associated protein that regulates wingless signaling in the embryonic epidermis. J Cell Biol 146, 1303-1318.
20. McCartney BM, Price MH, Webb RL, Hayden MA, Holot LM, Zhou M, Bejsovec A, Peifer M (2006). Testing hypotheses for the functions of APC family proteins using null and truncation alleles in Drosophila. Development 133, 2407-2418.
21. Minde DP, Anvarian Z, Rüdiger SG, Maurice MM (2011). Messing up disorder: how do missense mutations in the tumor suppressor protein APC lead to cancer? Mol Cancer 10, 101.
22. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P (1995). Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci USA 92, 3046-3050.
23. Nusse R (2012). Wnt signaling. Cold Spring Harb Perspect Biol 4, a011163.
24. Peterson-Nedry W, Erdeniz N, Kremer S, Yu J, Baig-Lewis S, Wehrli M (2008). Unexpectedly robust assembly of the Axin destruction complex regulates Wnt/Wg signaling in Drosophila as revealed by analysis in vivo. Dev Biol 320, 226-241.
25. Polakis P (2012). Wnt signaling in cancer. Cold Spring Harb Perspect Biol 4, a008052.
26. Pronobis MI, Rusan NM, Peifer M (2015). A novel GSK3-regulated APC:Axin interaction regulates Wnt signaling by driving a catalytic cycle of ef-fcient βcatenin destruction. eLife 4, e08022.
27. Roberts DM, Pronobis MI, Poulton JS, Kane EG, Peifer M (2012). Regulation of Wnt signaling by the tumor suppressor adenomatous polyposis coli does not require the ability to enter the nucleus or a particular cytoplas-mic localization. Mol Biol Cell 23, 2041-2056.
28. Roberts DM, Pronobis MI, Poulton JS, Waldmann JD, Stephenson EM, Hanna S, Peifer M (2011). Deconstructing the βcatenin destruction complex: mechanistic roles for the tumor suppressor APC in regulating Wnt signaling. Mol Biol Cell 22, 1845-1863.
29. Rubinfeld B, Albert I, Porfri E, Fiol C, Munemitsu S, Polakis P (1996). Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272, 1023-1026.
30. Rubinfeld B, Albert I, Porfri E, Munemitsu S, Polakis P (1997). Loss of beta-catenin regulation by the APC tumor suppressor protein correlates with loss of structure due to common somatic mutations of the gene. Cancer Res 57, 4624-4630.
31. Rubinfeld B, Souza B, Albert I, Munemitsu S, Polakis P (1995). The APC protein and E-cadherin form similar but independent complexes with alpha-catenin, beta-catenin, and plakoglobin. J Biol Chem 270, 5549-5555.
32. Rubinfeld B, Tice DA, Polakis P (2001). Axin-dependent phosphorylation of the adenomatous polyposis coli protein mediated by casein kinase 1epsilon. J Biol Chem 276, 39037-39045.
33. Schneikert J, Ruppert JG, Behrens J, Wenzel EM (2014). Different roles for the axin interactions with the SAMP versus the second twenty amino acid repeat of adenomatous polyposis coli. PLoS One 9, e94413.
34. Schneikert J, Vijaya Chandra SH, Ruppert JG, Ray S, Wenzel EM, Behrens J (2013). Functional comparison of human adenomatous polyposis coli (APC) and APC-like in targeting beta-catenin for degradation. PLoS One 8, e68072.
35. Sherwood V (2015). WNT signaling: an emerging mediator of cancer cell metabolism? Mol Cell Biol 35, 2-10.
36. Smits R, Kielman MF, Breukel C, Zurcher C, Neufeld K, Jagmohan-Changur S, Hofand N, van Dijk J, White R, Edelmann W, et al. (1999). Apc1638T: a mouse model delineating critical domains of the adenomatous poly-posis coli protein involved in tumorigenesis and development. Genes Dev 13, 1309-1321.
37. Spink KE, Polakis P, Weis WI (2000). Structural basis of the Axin-adenoma-tous polyposis coli interaction. EMBO J 19, 2270-2279.
38. Stamos JL, Weis WI (2013). The β-catenin destruction complex. Cold Spring Harb Perspect Biol 5, a007898.
39. Wieschaus E, Nusslein-Volhard C (1998). Drosophila: A Practical Approach, Oxford, UK: Oxford University Press.
40. Xing Y, Clements WK, Le Trong I, Hinds TR, Stenkamp R, Kimelman D, Xu W (2004). Crystal structure of a beta-catenin/APC complex reveals a critical role for APC phosphorylation in APC function. Mol Cell 15, 523-533.
41. Yamulla RJ, Kane EG, Moody AE, Politi KA, Lock NE, Foley AVA, Roberts DM (2014). Testing models of the APC tumor suppressor/β-catenin interaction reshapes our view of the destruction complex in Wnt signaling. Genetics 197, 1285-1302.
42. Zhai B, Villén J, Beausoleil SA, Mintseris J, Gygi SP (2008). Phosphopro-teome analysis of Drosophila melanogaster embryos. J Proteome Res 7, 1675-1682.
43. Zhou M-N, Kunttas-Tatli E, Zimmerman S, Zhouzheng F, McCartney BM (2011). Cortical localization of APC2 plays a role in actin organization but not in Wnt signaling in Drosophila. J Cell Sci 124, 1589-1600.