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

Volumn 25, Issue 21, 2014, Pages 3424-3436

  Kunttas Tatli, Ezgi ^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

APC PROTEIN; AXIN; BETA CATENIN; APC PROTEIN, HUMAN; APC2 PROTEIN, DROSOPHILA; ARMADILLO DOMAIN PROTEIN; ARMADILLO PROTEIN, DROSOPHILA; AXIN PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

AMINO TERMINAL SEQUENCE; APC SELF ASSOCIATION DOMAIN; ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; DROSOPHILA; EMBRYO; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN STRUCTURE; TURNOVER TIME; WNT SIGNALING PATHWAY; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; COLORECTAL TUMOR; CYTOLOGY; EMBRYOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NONMAMMALIAN EMBRYO; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; TRANSGENIC ANIMAL; TUMOR CELL LINE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARMADILLO DOMAIN PROTEINS; AXIN PROTEIN; BETA CATENIN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; WNT SIGNALING PATHWAY;

EID: 84908635494     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-04-0885     Document Type: Article

References (70)

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. Cadigan KM, Peifer M (2009). Wnt signaling from development to disease: insights from model systems. Cold Spring Harb Perspect Biol 1, a002881.
5. Carson DJ, Santoro IM, Groden J (2004). Isoforms of the APC tumor suppressor and their ability to inhibit cell growth and tumorigenicity. Oncogene 23, 7144-7148.
6. Chen T, Yang I, Irby R, Shain KH, Wang HG, Quackenbush J, Coppola D, Cheng JQ, Yeatman TJ (2003). Regulation of caspase expression and apoptosis by adenomatous polyposis coli. Cancer Res 63, 4368-4374.
7. Clevers H, Nusse R (2012). Wnt/β-catenin signaling and disease. Cell 149, 1192-1205.
8. Crist RC, Roth JJ, Baran AA, McEntee BJ, Siracusa LD, Buchberg AM (2010). The armadillo repeat domain of Apc suppresses intestinal tumorigenesis. Mamm Genome 21, 450-457.
9. 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.
10. 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.
11. 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.
12. Fodde R (2002). The APC gene in colorectal cancer. Eur J Cancer 38, 867-871.
13. Green RA, Kaplan KB (2003). Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J Cell Biol 163, 949-961.
14. Green RA, Wollman R, Kaplan KB (2005). APC and EB1 function together in mitosis to regulate spindle dynamics and chromosome alignment. Mol Biol Cell 16, 4609-4622.
15. Groden J, Thliveris A, Samowitz W, Carlson M, Gelbert L, Albertsen H, Joslyn G, Stevens J, Spirio L, Robertson M (1991). Identification and characterization of the familial adenomatous polyposis coli gene. Cell 66, 589-600.
16. Gruber M, Lupas AN (2003). Historical review: another 50th anniversary - new periodicities in coiled coils. Trends Biochem Sci 28, 679-685.
17. Guder C, Philipp I, Lengfeld T, Watanabe H, Hobmayer B, Holstein TW (2006). The Wnt code: cnidarians signal the way. Oncogene 25, 7450-7460.
18. 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.
19. 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, beta-catenin and GSK3 beta. Curr Biol 8, 573-581.
20. 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-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17, 1371-1384.
21. Jimbo T, Kawasaki Y, Koyama R, Sato R, Takada S, Haraguchi K, Akiyama T (2002). Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat Cell Biol 4, 323-327.
22. Joslyn G, Carlson M, Thliveris A, Albertsen H, Gelbert L, Samowitz W, Groden J, Stevens J, Spirio L, Robertson M (1991). Identification of deletion mutations and three new genes at the familial polyposis locus. Cell 66, 601-613.
23. Joslyn G, Richardson DS, White R, Alber T (1993). Dimer formation by an N-terminal coiled coil in the APC protein. Proc Natl Acad Sci USA 90, 11109-11113.
24. Kawasaki Y (2000). Asef, a link between the tumor suppressor APC and G-protein signaling. Science 289, 1194-1197.
25. Kim JH, Liu X, Wang J, Chen X, Zhang H, Kim SH, Cui J, Li R, Zhang W, Kong Y, et al. (2013). Wnt signaling in bone formation and its therapeutic potential for bone diseases. Ther Adv Musculoskelet Dis 5, 13-31.
26. Kimelman D, Xu W (2006). beta-Catenin destruction complex: insights and questions from a structural perspective. Oncogene 25, 7482-7491.
27. Kishida S, Yamamoto H, Hino S, 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. Mol Cell Biol 19, 4414-4422.
28. Komori H, Xiao Q, McCartney BM, Lee C-Y (2014). Brain tumor specifies intermediate progenitor cell identity by attenuating β-catenin/Armadillo activity. Development 141, 51-62.
29. 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.
30. 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.
31. Lee E, Salic A, Krüger R, Heinrich R, Kirschner MW (2003). The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol 1, E10.
32. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, Mohammed S, Heck AJ, Maurice MM, Mahmoudi T, et al. (2012). Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 149, 1245-1256.
33. Li Z, Kroboth K, Newton IP, Näthke IS (2008). Novel self-association of the APC molecule affects APC clusters and cell migration. J. Cell Sci 121, 1916-1925.
34. Li Z, Näthke IS (2005). Tumor-associated NH2-terminal fragments are the most stable part of the adenomatous polyposis coli protein and can be regulated by interactions with COOH-terminal domains. Cancer Res 65, 5195-5204.
35. Logan CY, Nusse R (2004). The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20, 781-810.
36. Luo W, Lin S-C (2004). Axin: a master scaffold for multiple signaling pathways. Neurosignals 13, 99-113.
37. Lupas A, Van Dyke M, Stock J (1991). Predicting coiled coils from protein sequences. Science 252, 1162-1164.
38. Mao J, Wang J, Liu B, Pan W, Farr GH, Flynn C, Yuan H, Takada S, Kimelman D, Li L, Wu D (2001). Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol Cell 7, 801-809.
39. Mattie FJ, Stackpole MM, Stone MC, Clippard JR, Rudnick DA, Qiu Y, Tao J, Allender DL, Parmar M, Rolls MM (2010). Directed microtubule growth, +TIPs, and kinesin-2 are required for uniform microtubule polarity in dendrites. Curr Biol 20, 2169-2177.
40. 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.
41. McCartney BM, Näthke IS (2008). Cell regulation by the Apc protein Apc as master regulator of epithelia. Curr Opin Cell Biol 20, 186-193.
42. 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.
43. Mendoza-Topaz C, Mieszczanek J, Bienz M (2011). The Adenomatous polyposis coli tumour suppressor is essential for Axin complex assembly and function and opposes Axin's interaction with Dishevelled. Open Biol 1, 110013.
44. Morishita EC, Murayama K, Kato-Murayama M, Ishizuka-Katsura Y, Tomabechi Y, Hayashi T, Terada T, Handa N, Shirouzu M, Akiyama T, Yokoyama S (2011). Crystal structures of the armadillo repeat domain of adenomatous polyposis coli and its complex with the tyrosine-rich domain of Sam68. Structure 19, 1496-1508.
45. 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.
46. 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 Cells 3, 395-403.
47. Nishisho I, Nakamura Y, Miyoshi Y, Miki Y, Ando H, Horii A, Koyama K, Utsunomiya J, Baba S, Hedge P (1991). Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. Science 253, 665-669.
48. Okada K, Bartolini F, Deaconescu AM, Moseley JB, Dogic Z, Grigorieff N, Gundersen GG, Goode BL (2010). Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J Cell Biol 189, 1087-1096.
49. Oliva CA, Vargas JY, Inestrosa NC (2013). Wnts in adult brain: from synaptic plasticity to cognitive deficiencies. Front Cell Neurosci 7, 224.
50. Polakis P (2007). The many ways of Wnt in cancer. Curr Opin Genet Dev 17, 45-51.
51. Polakis P (2012). Wnt signaling in cancer. Cold Spring Harb Perspect Biol 4, a008052.
52. 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 cytoplasmic localization. Mol Biol Cell 23, 2041-2056.
53. 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.
54. Rubinfeld B, Albert I, Porfiri 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.
55. Santoro IM, Groden J (1997). Alternative splicing of the APC gene and its association with terminal differentiation. Cancer Res 57, 488-494.
56. 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.
57. Schwarz-Romond T, Fiedler M, Shibata N, Butler PJG, Kikuchi A, Higuchi Y, Bienz M (2007a). The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat Struct Mol Biol 14, 484-492.
58. Schwarz-Romond T, Metcalfe C, Bienz M (2007b). Dynamic recruit ment of axin by Dishevelled protein assemblies. J Cell Sci 120, 2402-2412.
59. Seeling JM, Miller JR, Gil R, Moon RT, White R, Virshup DM (1999). Regulation of beta-catenin signaling by the B56 subunit of protein phosphatase 2A. Science 283, 2089-2091.
60. 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. Mol Cell 32, 652-661.
61. Thliveris A, Samowitz W, Matsunami N, Groden J, White R (1994). Demonstration of promoter activity and alternative splicing in the region 5′ to exon 1 of the APC gene. Cancer Res 54, 2991-2995.
62. Van der Luijt RB, Vasen HF, Tops CM, Breukel C, Fodde R, Meera Khan P (1995). APC mutation in the alternatively spliced region of exon 9 associated with late onset familial adenomatous polyposis. Hum Genet 96, 705-710.
63. Van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis A-P, et al. (2002). The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250.
64. Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K (2004). Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell 7, 871-883.
65. Welters HJ, Kulkarni RN (2008). Wnt signaling: relevance to beta-cell biology and diabetes. Trends Endocrinol Metab 19, 349-355.
66. Wieschaus E, Nusslein-Volhard C (1998). Drosophila: A Practical Approach, Oxford, UK: Oxford University Press.
67. Yamulla RJ, Kane EG, Moody AE, Politi KA, Lock NE, Foley AV, 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.
68. 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. J Biol Chem 281, 17751-17757.
69. Zhang Z, Chen L, Gao L, Lin K, Zhu L, Lu Y, Shi X, Gao Y, Zhou J, Xu P, et al. (2012). Structural basis for the recognition of Asef by adenomatous polyposis coli. Cell Res 22, 372-386.
70. 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.