A novel GSK3-regulated APC:Axin interaction regulates Wnt signaling by driving a catalytic cycle of efficient βcatenin destruction

eLife

Volumn 4, Issue September 2015, 2015, Pages

  Pronobis, Mira I ^a   Rusan, Nasser M ^b   Peifer, Mark ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; TANKYRASE INHIBITOR; WNT PROTEIN; APC PROTEIN;

ARTICLE; CELL CULTURE; CELL DESTRUCTION; COLON POLYPOSIS; DROSOPHILA; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE DELETION; GENE MUTATION; GENETIC TRANSFECTION; IMMUNOBLOTTING; MACROMOLECULE; MICROSCOPY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; RADIOACTIVITY; ANIMAL; CELL LINE; FLUORESCENCE MICROSCOPY; HUMAN; METABOLISM; PROTEIN ANALYSIS; PROTEIN DEGRADATION; WNT SIGNALING PATHWAY;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; AXIN PROTEIN; BETA CATENIN; CELL LINE; DROSOPHILA; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICROSCOPY, FLUORESCENCE; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEOLYSIS; WNT SIGNALING PATHWAY;

EID: 84943781425     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08022     Document Type: Article

References (54)

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 E, Price M, McCartney B, Hayden M, DeNofrio J, Peifer M. 2002. Drosophila APC2 and APC1 play overlapping roles in wingless signaling in the embryo and imaginal discs. Developmental Biology 250: 91-100. doi: 10.1006/dbio.2002.0776.
3. Albuquerque C, Breukel C, van der Luijt R, Fidalgo P, Lage P, Slors FJ, Leitao CN, Fodde R, Smits R. 2002. The ‘just-right’ signaling model: APC somatic mutations are selected based on a specific level of activation of the beta-catenin signaling cascade. Human Molecular Genetics 11:1549-1560. doi: 10.1093/hmg/11.13.1549.
4. Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M, Niehrs C. 2007. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316:1619-1622. doi: 10.1126/science.1137065.
5. Castellsague´ E, González S, Guiná E, Stevens KN, Borrá s E, Raymond VM, Lázaro C, Blanco I, Gruber SB, Capellá G. 2010. Allele-specific expression of APC in adenomatous polyposis families. Gastroenerology 139:439-447. doi: 10.1053/j.gastro.2010.04.047.
6. Choi SH, Estaras C, Moresco JJ, Yates JR, Jones KA. 2013. alpha-Catenin interacts with APC to regulate betacatenin proteolysis and transcriptional repression of Wnt target genes. Genes & Development 27:2473-2488. doi: 10.1101/gad.229062.113.
7. Chou TB, Perrimon N. 1996. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144:1673-1679.
8. Christie M, Jorissen RN, Mouradov D, Sakthianandeswaren A, Li S, Day F, Tsui C, Lipton L, Desai J, Jones IT, McLaughlin S, Ward RL, Hawkins NJ, Ruszkiewicz AR, Moore J, Burgess AW, Busam D, Zhao Q, Strausberg RL, Simpson AJ, Tomlinson IP, Gibbs P, Sieber OM. 2013. Different APC genotypes in proximal and distal sporadic colorectal cancers suggest distinct WNT/β-catenin signalling thresholds for tumourigenesis. Oncogene 32: 4675-4682. doi: 10.1038/onc.2012.486.
9. Clevers H, Nusse R. 2012. Wnt/beta-catenin signaling and disease. Cell 149:1192-1205. doi: 10.1016/j.cell.2012.05.012.
10. de la Roche M, Ibrahim AE, Mieszczanek J, Bienz M. 2014. LEF1 and B9L shield β-catenin from inactivation by Axin, desensitizing colorectal cancer cells to tankyrase inhibitors. Cancer Research 74:1495-1505. doi: 10.1158/0008-5472.CAN-13-2682.
11. Fagotto F, Jho EH, Zeng L, Kurth T, Joos T, Kaufmann C, Costantini F. 1999. Domains of Axin involved in proteinprotein interactions, Wnt pathway inhibition, and intracellular localization. The Journal of Cell Biology 145: 741-756. doi: 10.1083/jcb.145.4.741.
12. Faux MC, Coates JL, Catimel B, Cody S, Clayton AH, Layton MJ, Burgess AW. 2008. Recruitment of adenomatous polyposis coli and beta-catenin to axin-puncta. Oncogene 27:5808-5820. doi: 10.1038/onc.2008.205.
13. 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 beta-catenin. Proceedings of the National Academy of Sciences of USA 108:1937-1942. doi: 10.1073/pnas.1017063108.
14. Ha NC, Tonozuka T, Stamos JL, Choi HJ, Weis WI. 2004. Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Molecular Cell 15:511-521. doi: 10.1016/j.molcel.2004.08.010.
15. Hart MJ, de los Santos R, Albert IN, Rubinfeld B, Polakis P. 1998. Downregulation of beta-catenin by human Axin and its association with the APC tumor suppressor, β-catenin and GSK3β. Current Biology 8:573-581. doi: 10.1016/S0960-9822(98)70226-X.
16. Hernandez AR, Klein AM, Kirschner MW. 2012. Kinetic responses of beta-catenin specify the sites of Wnt control. Science 338:1337-1340. doi: 10.1126/science.1228734.
17. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A. 1998. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3β and β-catenin and promotes GSK-3β-dependent phosphorylation of β-catenin. The EMBO Journal 17:1371-1384. doi: 10.1093/emboj/17.5.1371.
18. Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, Xie M, Zhang Q, McMichael JF, Wyczalkowski MA, Leiserson MD, Miller CA, Welch JS, Walter MJ, Wendl MC, Ley TJ, Wilson RK, Raphael BJ, Ding L. 2013. Mutational landscape and significance across 12 major cancer types. Nature 502:333-339. doi: 10.1038/nature12634.
19. Kim SE, Huang H, Zhao M, Zhang X, Zhang A, Semonov MV, MacDonald BT, Zhang X, Garcia Abreu J, Peng L, He X. 2013. Wnt stabilization of beta-catenin reveals principles for morphogen receptor-scaffold assemblies. Science 340:867-870. doi: 10.1126/science.1232389.
20. Kishida S, Yamamoto H, Hino SI, Ikeda S, Kishida M, Kikuchi A. 1999. DIX domains of Dvl and axin are necessary for protein interactions and their ability to regulate beta-catenin stability. Molecular and Cellular Biology 19: 4414-4422.
21. Klein PS, Melton DA. 1996. A molecular mechanism for the effect of lithium on development. Proceedings of the National Academy of Sciences of USA 93:8455-8459. doi: 10.1073/pnas.93.16.8455.
22. Kohler EM, Chandra SH, Behrens J, Schneikert J. 2009. Beta-catenin degradation mediated by the CID domain of APC provides a model for the selection of APC mutations in colorectal, desmoid and duodenal tumours. Human Molecular Genetics 18:213-226. doi: 10.1093/hmg/ddn338.
23. Kohler EM, Derungs A, Daum G, Behrens J, Schneikert J. 2008. Functional definition of the mutation cluster region of adenomatous polyposis coli in colorectal tumours. Human Molecular Genetics 17:1978-1987. doi: 10.1093/hmg/ddn095.
24. 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. Molecular Biology of the Cell 25: 3424-3436. doi: 10.1091/mbc.E14-04-0885.
25. Lee E, Salic A, Kruger R, Heinrich R, Kirschner MW. 2003. The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLOS Biology 1:E10. doi: 10.1371/journal.pbio.0000010.
26. Li PL, Banjade S, Cheng HC, Kim S, Chen B, Guo L, Llaguno M, Hollingsworth JV, King DS, Banani SF, Russo PS, Jiang QX, Nixon BT, Rosen MK. 2012a. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336-U129. doi: 10.1038/nature10879.
27. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, Mohammed S, Heck AJ, Maurice MM, Mahmoudi T, Clevers H. 2012b. Wnt signaling through inhibition of beta-catenin degradation in an intact Axin1 complex. Cell 149:1245-1256. doi: 10.1016/j.cell.2012.05.002.
28. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. 2002. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837-847. doi: 10.1016/S0092-8674(02)00685-2.
29. 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. Journal of Molecular Biology 360:133-144. doi: 10.1016/j.jmb.2006.04.064.
30. MacDonald BT, He X. 2012. A finger on the pulse of Wnt receptor signaling. Cell Research 22:1410-1412. doi: 10.1038/cr.2012.91.
31. Maher MT, Flozak AS, Stocker AM, Chenn A, Gottardi CJ. 2009. Activity of the beta-catenin phosphodestruction complex at cell-cell contacts is enhanced by cadherin-based adhesion. The Journal of Cell Biology 186:219-228. doi: 10.1083/jcb.200811108.
32. 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. doi: 10.1242/dev.02398.
33. Meijer L, Skaltsounis AL, Magiatis P, Polychronopoulos P, Knockaert M, Leost M, Ryan XP, Vonica CA, Brivanlou A, Dajani R, Crovace C, Tarricone C, Musacchio A, Roe SM, Pearl L, Greengard P. 2003. GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chemistry & Biology 10:1255-1266. doi: 10.1016/j.chembiol.2003.11.010.
34. Mendoza-Topaz C, Mieszczanek J, Bienz M. 2011. The APC tumour suppressor is essential for Axin complex assembly and function, and opposes Axin’s interaction with Dishevelled. Biology Open 1:110013. doi: 10.1098/rsob.110013.
35. Nakamura T, Hamada F, Ishidate T, Anai K, Kawahara K, Toyoshima K, Akiyama T. 1998. Axin, an inhibitor of the Wnt signalling pathway, interacts with beta- catenin, GSK-3beta and APC and reduces the beta-catenin level. Genes To Cells 3:395-403. doi: 10.1046/j.1365-2443.1998.00198.x.
36. Nelson S, Nathke IS. 2013. Interactions and functions of the adenomatous polyposis coli (APC) protein at a glance. Journal of Cell Science 126:873-877. doi: 10.1242/jcs.100479.
37. Pai L-M, Orsulic S, Bejsovec A, Peifer M. 1997. Negative regulation of Armadillo, a Wingless effector in Drosophila. Development 124:2255-2266.
38. Polakis P. 2007. The many ways of Wnt in cancer. Current Opinion in Genetics & Development 17:45-51. doi: 10.1016/j.gde.2006.12.007.
39. Popp MW, Maquat LE. 2013. Organizing principles of mammalian nonsense-mediated mRNA decay. Annual Review of Genetics 47:139-165. doi: 10.1146/annurev-genet-111212-133424.
40. Roberts DM, Pronobis MI, Poulton JS, Kane EG, Peifer M. 2012. Regulation of Wnt signaling by the tumor suppressor APC does not require ability to enter the nucleus nor a particular cytoplasmic localization. Molecular Biology of the Cell 23:2041-2056. doi: 10.1091/mbc.E11-11-0965.
41. Roberts DM, Pronobis MI, Poulton JS, Waldmann JD, Stephenson EM, Hanna S, Peifer M. 2011. Deconstructing the beta-catenin destruction complex: mechanistic roles for the tumor suppressor APC in regulating Wnt signaling. Molecular Biology of the Cell 22:1845-1863. doi: 10.1091/mbc.E10-11-0871.
42. Rubinfeld B, Albert I, Porfiri E, Munemitsu S, Polakis P. 1997. Loss of β-catenin regulation by the APC tumor suppressor protein correlates with loss of structure due to common somatic mutations of the gene. Cancer Research 57:4624-4630.
43. Rubinfeld B, Tice DA, Polakis P. 2001. Axin-dependent phosphorylation of the adenomatous polyposis coli protein mediated by casein kinase 1epsilon. The Journal of Biological Chemistry 276:39037-39045. doi: 10.1074/jbc.M105148200.
44. Sadot E, Conacci-Sorrell M, Zhurinsky J, Shnizer D, Lando Z, Zharhary D, Kam Z, Ben-Ze’ev A, Geiger B. 2002. Regulation of S33/S37 phosphorylated beta-catenin in normal and transformed cells. Journal of Cell Science 115: 2771-2780.
45. Schagger H. 2006. Tricine-SDS-PAGE. Nature Protocols 1:16-22. doi: 10.1038/nprot.2006.4.
46. 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. doi: 10.1371/journal.pone.0094413.
47. Schwarz-Romond T, Fiedler M, Shibata N, Butler PJ, Kikuchi A, Higuchi Y, Bienz M. 2007. The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nature Structural & Molecular Biology 14:484-492. doi: 10.1038/nsmb1247.
48. Stambolic V, Ruel L, Woodgett JR. 1996. Lithium inhibits glycogen synthase kinase-3 activity and mimics Wingless signaling in intact cells. Current Biology 6:1664-1668. doi: 10.1016/S0960-9822(02)70790-2.
49. Su Y, Fu C, Ishikawa S, Stella A, Kojima M, Shitoh K, Schreiber EM, Day BW, Liu B. 2008. APC is essential for targeting phosphorylated beta-catenin to the SCFbeta-TrCP ubiquitin ligase. Molecular Cell 32:652-661. doi: 10.1016/j.molcel.2008.10.023.
50. Toretsky JA, Wright PE. 2014. Assemblages: functional units formed by cellular phase separation. The Journal of Cell Biology 206:579-588. doi: 10.1083/jcb.201404124.
51. Wieschaus E, Nusslein-Volhard C. 1998. Looking at embryos. In: Roberts DB, editor. Drosophila: a practical approach. Oxford: Oxford University Press. p. 179-214.
52. Yamamoto H, Kishida S, Kishida M, Ikeda S, Takada S, Kikuchi A. 1999. Phosphorylation of axin, a Wnt signal negative regulator, by glycogen synthase kinase-3beta regulates its stability. The Journal of Biological Chemistry 274:10681-10684. doi: 10.1074/jbc.274.16.10681.
53. Yamulla RJ, Kane EG, Moody AE, Politi KA, Lock NE, Foley AV, Roberts DM. 2014. Testing models of the APC tumor suppressor/beta-catenin interaction reshapes our view of the destruction complex in Wnt signaling. Genetics 197:1285-1302. doi: 10.1534/genetics.114.166496.
54. Yang J, Zhang W, Evans PM, Chen X, He X, Liu C. 2006. Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. The Journal of Biological Chemistry 281: 17751-17757. doi: 10.1074/jbc.M600831200.