Threonine 393 of β-catenin regulates interaction with axin

Journal of Cellular Biochemistry

Volumn 108, Issue 1, 2009, Pages 52-63

  Wu, Hao ^a   Symes, Karen ^a   Seldin, David C ^a   Dominguez, Isabel ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE   (United States)

Author keywords

catenin phosphorylation; catenin stability; AXIN; CK2; E Cadherin; GSK3 ; Wnt signaling

Indexed keywords

AXIN; BETA CATENIN; CASEIN KINASE II; GLYCOGEN SYNTHASE KINASE 3BETA; THREONINE; UVOMORULIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

ANIMALS; BETA CATENIN; BINDING SITES; CADHERINS; CELLS, CULTURED; EMBRYO, NONMAMMALIAN; HUMANS; MUTATION; PHOSPHORYLATION; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; THREONINE; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; XENOPUS; XENOPUS PROTEINS;

XENOPUS LAEVIS;

EID: 69249100142     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22260     Document Type: Article

References (81)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. 1997. Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797-3804.
2. Ahmad KA, Wang G, Unger G, Slaton J, Ahmed K. 2008. Protein kinase CK2-A key suppressor of apoptosis. Adv Enzyme Regul 48:179-187.
3. Allada R, Meissner RA. 2005. Casein kinase 2, circadian clocks, and the flight from mutagenic light. Mol Cell Biochem 274:141-149.
4. Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M, Ben-Neriah Y, Alkalay I. 2002. Axin-mediated CKI phosphorylation of betacatenin at Ser 45: A molecular switch for the Wnt pathway. Genes Dev 16:1066-1076.
5. Bek S, Kemler R. 2002. Protein kinase CKII regulates the interaction of beta-catenin with alpha-catenin and its protein stability. J Cell Sci 115:4743-4753.
6. Bernard P, Fleming A, Lacombe A, Harley VR, Vilain E. 2008. Wnt4 inhibits beta-catenin/TCF signaling by redirecting beta-catenin to the cell membrane. Biol Cell 100:167-177.
7. Bosc DG, Luscher B, Litchfield DW. 1999. Expression and regulation of protein kinase CK2 during the cell cycle. Mol Cell Biochem 191:213-222.
8. Bryja VE, Schambony A, Cajanek LS, Dominguez I, Arenas E, Schulte G. 2008. Beta-Arrestin and casein kinase 1/2 define distinct branches of noncanonical WNT signalling pathways. EMBO Rep 9:1244-1250.
9. Buchou T, Vernet M, Blond O, Jensen HH, Pointu H, Olsen BB, Cochet C, Issinger OG, Boldyreff B. 2003. Disruption of the regulatory beta subunit of protein kinase CK2 in mice leads to a cell-autonomous defect and early embryonic lethality. Mol Cell Biol 23:908-915.
10. Canton DA, Litchfield DW. 2006. The shape of things to come: An emerging role for protein kinase CK2 in the regulation of cell morphology and the cytoskeleton. Cell Signal 18:267-275.
11. Catimel B, Layton M, Church N, Ross J, Condron M, Faux M, Simpson RJ, Burgess AW, Nice EC. 2006. In situ phosphorylation of immobilized receptors on biosensor surfaces: Application to E-cadherin/beta-catenin interactions. Anal Biochem 357:277-288.
12. Chen RH, Ding WV, McCormick F. 2000. Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. J Biol Chem 275:17894-17899.
13. Choi HJ, Huber AH, Weis WI. 2006. Thermodynamics of beta-catenin-ligand interactions: The roles of the N- and C-terminal tails in modulating binding affinity. J Biol Chem 281:1027-1038.
14. Cox RT, Pai LM, Miller JR, Orsulic S, Stein J, McCormick CA, Audeh Y, Wang W, Moon RT, Peifer M. 1999. Membrane-tethered Drosophila Armadillo cannot transduce Wingless signal on its own. Development 126:1327-1335.
15. Currier N, Solomon SE, Demicco EG, Chang DL, Farago M, Ying H, Dominguez I, Sonenshein GE, Cardiff RD, Xiao ZX, Sherr DH, Seldin DC. 2005. Oncogenic signaling pathways activated in DMBA-induced mouse mammary tumors. Toxicol Pathol 33:726-737.
16. Daugherty RL, Gottardi CJ. 2007. Phospho-regulation of Beta-catenin adhesion and signaling functions. Physiology (Bethesda) 22:303-309.
17. Dominguez I, Mizuno J, Wu H, Song DH, Symes K, Seldin DC. 2004. Protein kinase CK2 is required for dorsal axis formation in Xenopus embryos. Dev Biol 274:110-124.
18. Dominguez I, Mizuno J, Wu H, Imbrie GA, Symes K, Seldin DC. 2005. A role for CK2alpha/beta in Xenopus early embryonic development. Mol Cell Biochem 274:125-131.
19. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, Lu Z. 2007. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 282:11221-11229.
20. Fukui A, Kishida S, Kikuchi A, Asashima M. 2000. Effects of rat Axin domains on axis formation in Xenopus embryos. Dev Growth Differ 42:489-498.
21. Gao Y, Wang HY. 2006. Casein kinase 2 Is activated and essential for Wnt/beta-catenin signaling. J Biol Chem 281:18394-18400.
22. Giarre M, Semenov MV, Brown AM. 1998. Wnt signaling stabilizes the dualfunction protein beta-catenin in diverse cell types. Ann NY Acad Sci 857:43-55.
23. Gordon MD, Nusse R. 2006. Wnt signaling: Multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 281:22429-22433.
24. Gottardi CJ, Gumbiner BM. 2004. Distinct molecular forms of beta-catenin are targeted to adhesive or transcriptional complexes. J Cell Biol 167:339-349.
25. Gottardi CJ, Wong E, Gumbiner BM. 2001. E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J Cell Biol 153:1049-1060.
26. Guerra B, Issinger OG. 1999. Protein kinase CK2 and its role in cellular proliferation, development and pathology. Electrophoresis 20:391-408.
27. Gumbiner BM. 2000. Regulation of cadherin adhesive activity. J Cell Biol 148:399-404.
28. Gyenis L, Litchfield DW. 2008. The emerging CK2 interactome: Insights into the regulation and functions of CK2. Mol Cell Biochem 316:5-14.
29. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R. 1995. Lack of beta-catenin affects mouse development at gastrulation. Development 121:3529-3537.
30. Hagen T, Sethi JK, Foxwell N, Vidal-Puig A. 2004. Signalling activity of beta-catenin targeted to different subcellular compartments. Biochem J 379:471-477.
31. Hammerlein A, Weiske J, Huber O. 2005. A second protein kinase CK1-mediated step negatively regulates Wnt signalling by disrupting the lymphocyte enhancer factor-1/beta-catenin complex. Cell Mol Life Sci 62:606-618.
32. Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, Kintner C, Noro CY, Wylie C. 1994. Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79:791-803.
33. Hildesheim J, Salvador JM, Hollander MC, Fornace AJ, Jr. 2005. Casein kinase 2- and protein kinase A-regulated adenomatous polyposis coli and beta-catenin cellular localization is dependent on p38 MAPK. J Biol Chem 280:17221-17226.
34. Homma MK, Homma Y. 2005. Regulatory role of CK2 during the progression of cell cycle. Mol Cell Biochem 274:47-52.
35. Homma MK, Homma Y. 2008. Cell cycle and activation of CK2. Mol Cell Biochem 316:49-55.
36. Homma MK, Li D, Krebs EG, Yuasa Y, Homma Y. 2002. Association and regulation of casein kinase 2 activity by adenomatous polyposis coli protein. Proc Natl Acad Sci USA 99:5959-5964.
37. Huang H, He X. 2008. Wnt/beta-catenin signaling: New (and old) players and new insights. Curr Opin Cell Biol 20:119-125.
38. Huber AH, Weis WI. 2001. The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell 105:391-402.
39. Huber AH, Nelson WJ, Weis WI. 1997. Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell 90:871-882.
40. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W. 2000. Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 148:567-578.
41. 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.
42. Julius MA, Rai SD, Kitajewski J. 1999. Chimeric Wnt proteins define the amino-terminus of Wnt-1 as a transformation-specific determinant. Oncogene 18:149-156.
43. Kao KR, Elinson RP. 1988. The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev Biol 127:64-77.
44. Landesman-Bollag E, Romieu-Mourez R, Song DH, Sonenshein GE, Cardiff RD, Seldin DC. 2001. Protein kinase CK2 in mammary gland tumorigenesis. Oncogene 20:3247-3257.
45. 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 Biol 1:E10.
46. Lickert H, Bauer A, Kemler R, Stappert J. 2000. Casein kinase II phosphorylation of E-cadherin increases E-cadherin/beta-catenin interaction and strengthens cell-cell adhesion. J Biol Chem 275:5090-5095.
47. Litchfield DW. 2003. Protein kinase CK2: Structure, regulation and role in cellular decisions of life and death. Biochem J 369:1-15.
48. Liu X, Rubin JS, Kimmel AR. 2005. Rapid, Wnt-induced changes in GSK3beta associations that regulate beta-catenin stabilization are mediated by Galpha proteins. Curr Biol 15:1989-1997.
49. Lou DY, Dominguez I, Toselli P, Landesman-Bollag E, O'Brien C, Seldin DC. 2008. The alpha catalytic subunit of protein kinase CK2 is required for mouse embryonic development. Mol Cell Biol 28:131-139.
50. Luo W, Peterson A, Garcia BA, Coombs G, Kofahl B, Heinrich R, Shabanowitz J, Hunt DF, Yost HJ, Virshup DM. 2007. Protein phosphatase 1 regulates assembly and function of the beta-catenin degradation complex. EMBO J 26:1511-1521.
51. Meggio F, Pinna LA. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349-368.
52. Miller JR, Moon RT. 1997. Analysis of the signaling activities of localization mutants of beta- catenin during axis specification in Xenopus. J Cell Biol 139:229-243.
53. Miravet S, Piedra J, Miro F, Itarte E, Garcia de Herreros A, Dunach M. 2002. The transcriptional factor Tcf-4 contains different binding sites for betacatenin and plakoglobin. J Biol Chem 277:1884-1891.
54. Moon RT, Kohn AD, De Ferrari GV, Kaykas A. 2004. WNT and beta-catenin signalling: Diseases and therapies. Nat Rev Genet 5:691-701.
55. Newport J, Kirschner M. 1982. A major developmental transition in early Xenopus embryos. I. characterization and timing of cellular changes at the midblastula stage. Cell 30:675-686.
56. Nieuwkoop PD, Faber J. 1967. Normal table of Xenopus laevis. Amsterdam: North-Holland Publishing Company.
57. Nusse R. 2005. Wnt signaling in disease and in development. Cell Res 15:28-32.
58. Olmeda D, Castel S, Vilaro S, Cano A. 2003. Beta-catenin regulation during the cell cycle: Implications in G2/M and apoptosis. Mol Biol Cell 14:2844-2860.
59. Orsulic S, Huber O, Aberle H, Arnold S, Kemler R. 1999. E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1- mediated transactivation. J Cell Sci 112:1237-1245.
60. Papkoff J. 1997. Regulation of complexed and free catenin pools by distinct mechanisms. Differential effects of Wnt-1 and v-Src. J Biol Chem 272:4536-4543.
61. Provost E, Rimm DL. 1999. Controversies at the cytoplasmic face of the cadherin-based adhesion complex. Curr Opin Cell Biol 11:567-572.
62. Reya T, Clevers H. 2005. Wnt signalling in stem cells and cancer. Nature 434:843-850.
63. Seldin DC, Landesman-Bollag E, Farago M, Currier N, Lou D, Dominguez I. 2005. CK2 as a positive regulator of Wnt signalling and tumourigenesis. Mol Cell Biochem 274:63-67.
64. Serres M, Filhol O, Lickert H, Grangeasse C, Chambaz EM, Stappert J, Vincent C, Schmitt D. 2000. The disruption of adherens junctions is associated with a decrease of E-cadherin phosphorylation by protein kinase CK2. Exp Cell Res 257:255-264.
65. Shibamoto S, Higano K, Takada R, Ito F, Takeichi M, Takada S. 1998. Cytoskeletal reorganization by soluble Wnt-3a protein signalling. Genes Cells 3:659-670.
66. Sokol SY. 1999. Wnt signaling and dorso-ventral axis specification in vertebrates. Curr Opin Genet Dev 9:405-410.
67. Somorjai IM, Martinez-Arias A. 2008. Wingless signalling alters the levels, subcellular distribution and dynamics of Armadillo and E-cadherin in third instar larval wing imaginal discs. PLoS ONE 3:e2893.
68. Song DH, Sussman DJ, Seldin DC. 2000. Endogenous protein kinase CK2 participates in Wnt Signaling in mammary epithelial cells. J Biol Chem 275:23790-23797.
69. Song DH, Dominguez I, Mizuno J, Kaut M, Mohr SC, Seldin DC. 2003. CK2 phosphorylation of the armadillo repeat region of beta-catenin potentiates Wnt signaling. J Biol Chem 278:24018-24025.
70. Staal FJ, Burgering BM, van de Wetering M, Clevers HC. 1999. Tcf-1-mediated transcription in T lymphocytes: Differential role for glycogen synthase kinase-3 in fibroblasts and T cells. Int Immunol 11:317-323.
71. Strovel ET, Wu D, Sussman DJ. 2000. Protein phosphatase 2Calpha dephosphorylates axin and activates LEF-1-dependent transcription. J Biol Chem 275:2399-2403.
72. Tapia JC, Torres VA, Rodriguez DA, Leyton L, Quest AF. 2006. Casein kinase 2 (CK2) increases survivin expression via enhanced beta-catenin-T cell factor/ lymphoid enhancer binding factor-dependent transcription. Proc Natl Acad Sci USA 103:15079-15084.
73. Tolwinski NS, Wehrli M, Rives A, Erdeniz N, DiNardo S, Wieschaus E. 2003. Wg/Wnt signal can be transmitted through arrow/LRP5,6 and Axin independently of Zw3/Gsk3beta activity. Dev Cell 4:407-418.
74. Vaidya AB, Lasfargues EY, Sheffield JB, Coutinho WG. 1978. Murine mammary tumor virus (MuMTV) infection of an epithelial cell line established from C57BL/6 mouse mammary glands. Virology 90:12-22.
75. Waltzer L, Bienz M. 1999. The control of beta-catenin and TCF during embryonic development and cancer. Cancer Metastasis Rev 18:231-246.
76. Wang S, Jones KA. 2006. CK2 controls the recruitment of Wnt regulators to target genes in vivo. Curr Biol 16:2239-2244.
77. Willert K, Brink M, Wodarz A, Varmus H, Nusse R. 1997. Casein kinase 2 associates with and phosphorylates dishevelled. EMBO J 16:3089-3096.
78. Xu X, Toselli PA, Russell LD, Seldin DC. 1999. Globozoospermia in mice lacking the casein kinase II alpha' catalytic subunit. Nat Genet 23:118-121.
79. Yanagawa S, Matsuda Y, Lee JS, Matsubayashi H, Sese S, Kadowaki T, Ishimoto A. 2002. Casein kinase I phosphorylates the Armadillo protein and induces its degradation in Drosophila. EMBO J 21:1733-1742.
80. Zeng L, Fagotto F, Zhang T, Hsu W, Vasicek TJ, Perry WL 3rd, Lee JJ, Tilghman SM, Gumbiner BM, Costantini F. 1997. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90:181-192.
81. Zhang F, White RL, Neufeld KL. 2001. Cell density and phosphorylation control the subcellular localization of adenomatous polyposis coli protein. Mol Cell Biol 21:8143-8156.