α-Catenin interacts with APC to regulate β-catenin proteolysis and transcriptional repression of Wnt target genes

Genes and Development

Volumn 27, Issue 22, 2013, Pages 2473-2488

  Choi, Seung H ^a   Estarás, Conchi ^a   Moresco, James J ^b   Yates III, John R ^b   Jones, Katherine A ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

catenin; catenin; APC tumor suppressor; CtBP:RCOR1:LSD1; Transcription; Wnt signaling

Indexed keywords

ALPHA CATENIN; BETA CATENIN; COLON POLYPOSIS PROTEIN; LYMPHOID ENHANCER FACTOR 1; PROTEIN; UNCLASSIFIED DRUG; WNT3A PROTEIN;

ARTICLE; CELL JUNCTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; EMBRYO; EMBRYONIC STEM CELL; GENE REPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; TISSUE DIFFERENTIATION; TRANSCRIPTION REGULATION; UBIQUITINATION;

Α-CATENIN; Β-CATENIN; APC TUMOR SUPPRESSOR; CTBP:RCOR1:LSD1; TRANSCRIPTION; WNT SIGNALING;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ALPHA CATENIN; BETA CATENIN; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HCT116 CELLS; HEK293 CELLS; HUMANS; PROTEIN BINDING; PROTEOLYSIS; SIGNAL TRANSDUCTION; UBIQUITINATION; WNT PROTEINS;

EID: 84887599280     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.229062.113     Document Type: Article

References (48)

1. Alarcón C, Zaromytidou AI, Xi Q, Gao S, Yu J, Fujisawa S, Barlas A, Miller AN, Manova-Todorova K, Macias MJ, et al. 2009. Nuclear C. DKs drive Smad transcriptional activation and turnover in BMP and TGF-β pathways. Cell 139: 757-769.
2. Aoki K., Taketo MM. 2007. Adenomatous polyposis coli (APC): A multi-functional tumor suppressor gene. J Cell Sci 120: 3327-3335.
3. Aragon E., Goerner N, Zaromytidou AI, Xi Q, Escobedo A, Massague J., Macias MJ. 2011. A Smad action turnover switch operated by WW domain readers of a phosphoserine code. Genes Dev 25: 1275-1288.
4. Atilla-Gokcumen GE, Williams DS, Bregman H, Pagano N, Meggers E. 2006. Organometallic compounds with biological activity: A very selective and highly potent cellular inhibitor for glycogen synthase kinase 3. ChemBioChem 7: 1443-1450.
5. Azzolin L., Zanconato F, Bresolin S, Forcato M, Basso G, Bicciato S, Cordenonsi M, Piccolo S. 2012. Role of TAZ as mediator of Wnt signaling. Cell 151: 1443-1456.
6. Benjamin J. M, Nelson WJ. 2008. Bench to bedside and back again: Molecular mechanisms of α-catenin function and roles in tumorigenesis. Semin Cancer Biol 18: 53-64.
7. Benjamin J. M, Kwiatkowski AV, Yang C, Korobova F, Pokutta S, Svitkina T., Weis WI, Nelson WJ. 2008. αE-catenin regulates actin dynamics independently of cadherin-mediated cell-cell adhesion. J Cell Biol 189: 339-352.
8. Caldwell C. M, Kaplan KB. 2009. The role of APC in mitosis and chromosome instability. Adv Exp Med Biol 656: 51-64.
9. Chinnadurai G. 2009. The transcriptional corepressor CtBP: A foe of tumor suppressors. Cancer Res 69: 731-734.
10. Clevers H., Nusse R. 2012. Wnt/β-catenin signaling and disease. Cell 149: 1192-1205.
11. Fang M., Li J, Blauwkamp T, Bhambhani C, Campbell N, Cadigan KM. 2006. C-terminal binding protein directly activates and represses Wnt transcriptional targets in Drosophila. EMBO J 25: 2735-2745.
12. Fiedler M., Sánchez-Barrena MJ, Nekrasov M, Mieszczanek J, Rybin V., Müller J, Evans P, Bienz M. 2008. Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol Cell 30: 507-518.
13. Geng F., Wenzel S, Tansey WP. 2012. Ubiquitin and proteasomes in transcription. Annu Rev Biochem 81: 177-201.
14. Gieni R. S, Hendzel MJ. 2009. Actin dynamics and functions in the interphase nucleus: Moving towards an understanding of nuclear polymeric actin. Biochem Cell Biol 87: 283-306.
15. Ha N. C, Tonozuka T, Stamos JL, Choi HJ, Weis WI. 2004. Mechanism of phosphorylation-dependent binding of APC to β-catenin and its role in β-catenin degradation. Mol Cell 15: 511-521.
16. Hamada F., Bienz M. 2004. The APC tumor suppressor binds to C-terminal binding protein to divert nuclear β-catenin from TCF. Dev Cell 7: 677-685.
17. Hammoud S. S, Cairns BR, Jones DA. 2013. Epigenetic regulation of colon cancer and intestinal stem cells. Curr Opin Cell Biol 25: 177-183.
18. Huber O., Krohn M, Kemler R. 1997. A specific domain in α-catenin mediates binding to β-catenin or plakoglobin. J Cell Sci 110: 1759-1765.
19. Imajo M., Miyatake K, Iimura A, Miyamoto A, Nishida E. 2012. A molecular mechanism that links Hippo signalling to the inhibition of Wnt/β-catenin signalling. EMBO J 31: 1109-1122.
20. Inge L. J, Rajasekaran SA, Wolle D, Barwe SP, Ryazantsev S, Ewing C. M, Isaacs WB, Rajasekaran AK. 2008. α-Catenin overrides Src-dependent activation of β-catenin oncogenic signaling. Mol Cancer Ther 7: 1368-1397.
21. Jeong W. J, Yoon J, Park JC, Lee SH, Kaduwal S, Kim H, Yoon JB, Choi K.Y. 2012. Ras stabilization through aberrant activation of Wnt/β-catenin signaling promotes intestinal tumorigenesis. Sci Signal 5: ra30.
22. Ji H., Wang J, Nika H, Hawke D, Keezer S, Ge Q, Fang B, Fang X, Fang D., Litchfield DW, et al. 2009. EGF-induced ERK activation promotes CK2-mediated disassociation of α-catenin from β-catenin and transactivation of β-catenin. Mol Cell 36: 547-559.
23. Kim S. E, Huang H, Zhao M, Zhang X, Zhang A, Semonov MV, MacDonald BT, Zhang X, Garcia Abreu J, Poeng L, et al. 2013. Wnt stabilization of β-catenin reveals principles for morphogen receptor-scaffold assemblies. Science 340: 867-870.
24. Kohler E. M, Chandra SH, Behrens J, Schneikert J. 2009. β-Catenin degradation mediated by the CID domain of APC provides a model for the selection of APC mutations in colorectal, desmoids, and duodenal tumours. Hum Mol Genet 18: 213-226.
25. Layton M. J, Faux MC, Church NL, Catimel B, Kershaw NJ, Kapp EA, Nowell C, Coates JL, Burgess AW, Simpson RJ. 2012. Identification of a Wnt-induced protein complex by affinity proteomics using an antibody that recognizes a sub-population of β-catenin. Biochim Biophys Acta 1824: 925-937.
26. Li J., Wang CY. 2008. TBL1:TBLR1 and β-catenin recruit each other to Wnt target-gene promoter for transcription activation and oncogenesis. Nat Cell Biol 10: 160-169.
27. Li V. S, 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.
28. Lui C., Mills K, Brocardo MG, Sharma M, Henderson BR. 2012. APC as a mobile scaffold: Regulation and function at the nucleus, cytoplasm andmitochondria. IUBMB Life 64: 209-214.
29. McCartney B. M, Näthke IS. 2008. Cell regulation by the Apc protein: Apc as master regulator of epithelia. Curr Opin Cell Biol 20: 186-193.
30. Perissi V., Scafoglio C, Zhang J, Ohgi KA, Rose DW, Glass CK, Rosenfeld M.G. 2008. TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR/ SMRT transcriptional repression checkpoints. Mol Cell 29: 755-766.
31. Phelps R. A, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K., Broadbent T, Sarkar S, Burt RW, Jones DA. 2009. A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137: 623-634.
32. Rai K., Sarkar S, Broadbent TJ, Voas M, Grossmann KF, Nadauld LD, Dehghanizadeh S, Hagos FT, Li Y, Toth RK, et al. 2010. DNA demethylase activity maintains intestinal cells in an undifferentiated state following the loss of APC. Cell 142: 930-942.
33. Roberts D. M, PronobisMI, Poulton JS, Waldmann JD, Stephenson EM, Hanna S, Peifer M. 2011. Deconstructing the β-catenin destruction complex: Mechanistic roles for the tumor suppressor APC in regulating Wnt signaling. Mol Biol Cell 22: 1845-1863.
34. Robinson B. S, Moberg KH. 2011. Cell-cell junctions: α-Catenin and E-cadherin help fence in Yap1. Curr Biol 21: R890-R892.
35. Rosenbluh J., Nijhawan D, Cox AG, Li X, Neal JT, Schafer EJ, Zack T. I, Wang X, Tsherniak A, Schinzel AC, et al. 2012. β-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 151: 1457-1473.
36. Schlegelmilch K., Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D., Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, et al. 2011. Yap1 acts downstream of α-catenin to control epidermal proliferation. Cell 144: 782-795.
37. Sierra J., Yoshida T, Joazeiro CA, Jones KA. 2006. The APC tumor suppressor counteracts β-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev 20: 586-600.
38. Silvis M. R, Kreger BT, Lien WH, Klezovitch O, Rudakova GM, Camargo F. D, Lantz DM, Seykora JT, Vasioukhin V. 2011. α-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 4: ra33.
39. Stamos J. L, Weis WI. 2013. The β-catenin destruction complex. Cold Spring Harb Perspect Biol 5: a007898.
40. Su L. K, Vogelstein B, Kinzler KW. 1993. Association of the APC tumor suppressor with catenins. Science 262: 1734-1737.
41. 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 β-catenin to the SCF βTrCP ubiquitin ligase. Mol Cell 32: 652-661.
42. Tsai B. P, Hoverter NP, Waterman ML. 2012. Blending Hippo and WNT: Sharing messengers and regulation. Cell 151: 1401-1403.
43. Valenta T., Hausmann G, Basler K. 2012. The many faces and functions of β-catenin. EMBO J 31: 2714-2736.
44. Vasioukhin V., Bauer C, Degenstein L, Wise B, Fuchs E. 2001. Hyperproliferation and defects in epithelial polarity upon conditional ablation of α-catenin in skin. Cell 104: 605-617.
45. Wang Z., Song J, Milne TA, Wang GG, Li H, Allis CD, Patel DJ. 2010. Pro isomerization in MLL1 PHD3-bromo cassette connects H3K4me readout to CyP33 and HDAC-mediated repression. Cell 141: 1183-1194.
46. Wray J., Hartmann C. 2012. WNTing embryonic stem cells. Trends Cell Biol 22: 159-168.
47. Yu F. X, Guan KL. 2013. The Hippo pathway: Regulators and regulations. Genes Dev 27: 355-371.
48. Yu F. X, Zhao B, Panupinthu N, Jewell JL, Lian I, Wang LH, Zhao J, Yuan H, Tumaneng K, Li H, et al. 2012. Regulation of the Hippo-YAP pathway by G-protein coupled receptor signaling. Cell 150: 780-791.