Smurf1-mediated lys29-linked nonproteolytic polyubiquitination of axin negatively regulates wnt/β-catenin signaling

Molecular and Cellular Biology

Volumn 33, Issue 20, 2013, Pages 4095-4105

  Fei, Cong ^a   Li, Zhenfei ^a   Li, Chen ^a   Chen, Yuelei ^a   Chen, Zhangcheng ^a   He, Xiaoli ^a   Mao, Li ^a   Wang, Xin ^a   Zeng, Rong ^a   Li, Lin ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; BETA CATENIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; LYSINE; SMAD UBIQUITINATION REGULATORY FACTOR 1; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME DEGRADATION; FIBROBLAST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; AXIN PROTEIN; BETA CATENIN; FIBROBLASTS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-5; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; LYSINE; MICE; MUTATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; WNT PROTEINS;

EID: 84886921317     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00418-13     Document Type: Article

References (40)

1. Chen ZJ, Sun LJ. 2009. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33:275-286.
2. Komander D, Rape M. 2012. The ubiquitin code. Annu. Rev. Biochem. 81:203-229.
3. Tauriello DV, Maurice MM. 2010. The various roles of ubiquitin in Wnt pathway regulation. Cell Cycle 9:3700-3709.
4. Hicke L. 2001. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2:195-201.
5. Kulathu Y, Komander D. 2012. Atypical ubiquitylation-the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 13:508-523.
6. Bernassola F, Karin M, Ciechanover A, Melino G. 2008. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 14:10-21.
7. Zhang Y, Chang C, Gehling DJ, Hemmati-Brivanlou A, Derynck R. 2001. Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc. Natl. Acad. Sci. U. S. A. 98:974-979.
8. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH. 1999. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400:687-693.
9. Narimatsu M, Bose R, Pye M, Zhang L, Miller B, Ching P, Sakuma R, Luga V, Roncari L, Attisano L, Wrana JL. 2009. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137:295-307.
10. Wang HR, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, Thomsen GH, Wrana JL. 2003. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302:1775-1779.
11. Yamashita M, Ying SX, Zhang GM, Li C, Cheng SY, Deng CX, Zhang YE. 2005. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 121:101-113.
12. Fukunaga E, Inoue Y, Komiya S, Horiguchi K, Goto K, Saitoh M, Miyazawa K, Koinuma D, Hanyu A, Imamura T. 2008. Smurf2 induces ubiquitin-dependent degradation of Smurf1 to prevent migration of breast cancer cells. J. Biol. Chem. 283:35660-35667.
13. Clevers H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127:469-480.
14. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20:781-810.
15. Zhang Y, Liu S, Mickanin C, Feng Y, Charlat O, Michaud GA, Schirle M, Shi X, Hild M, Bauer A, Myer VE, Finan PM, Porter JA, Huang SM, Cong F. 2011. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat. Cell Biol. 13:623-629.
16. Kim S, Jho EH. 2010. The protein stability of Axin, a negative regulator of Wnt signaling, is regulated by Smad ubiquitination regulatory factor 2 (Smurf2). J. Biol. Chem. 285:36420-36426.
17. Tauriello DV, Haegebarth A, Kuper I, Edelmann MJ, Henraat M, Canninga-van Dijk MR, Kessler BM, Clevers H, Maurice MM. 2010. Loss of the tumor suppressor CYLD enhances Wnt/beta-catenin signaling through K63-linked ubiquitination of Dvl. Mol. Cell 37:607-619.
18. Tran H, Bustos D, Yeh R, Rubinfeld B, Lam C, Shriver S, Zilberleyb I, Lee MW, Phu L, Sarkar AA, Zohn IE, Wertz IE, Kirkpatrick DS, Polakis P. 2013. HectD1 E3 ligase modifies adenomatous polyposis coli (APC) with polyubiquitin to promote the APC-axin interaction. J. Biol. Chem. 288:3753-3767.
19. Hay-Koren A, Caspi M, Zilberberg A, Rosin-Arbesfeld R. 2011. The EDD E3 ubiquitin ligase ubiquitinates and up-regulates beta-catenin. Mol. Biol. Cell 22:399-411.
20. Chen T, Li M, Ding Y, Zhang LS, Xi Y, Pan WJ, Tao DL, Wang JY, Li L. 2009. Identification of zinc-finger BED domain-containing 3 (Zbed3) as a novel Axin-interacting protein that activates Wnt/beta-catenin signaling. J. Biol. Chem. 284:6683-6689.
21. Chen YL, Liu B, Zhou ZN, Hu RY, Fei C, Xie ZH, Ding X. 2009. Smad6 inhibits the transcriptional activity of Tbx6 by mediating its degradation. J. Biol. Chem. 284:23481-23490.
22. Li L, Yuan H, Weaver CD, Mao J, Farr GH, III, Sussman DJ, Jonkers J, Kimelman D, Wu D. 1999. Axin and Frat1 interact with dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1. EMBO J. 18:4233-4240.
23. Mao J, Wang J, Liu B, Pan W, Farr GH, III, Flynn C, Yuan H, Takada S, Kimelman D, Li L, Wu D. 2001. Low-density lipoprotein receptorrelated protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol. Cell 7:801-809.
24. Li S, Lu K, Wang J, An L, Yang G, Chen H, Cui Y, Yin X, Xie P, Xing G, He F, Zhang L. 2010. Ubiquitin ligase Smurf1 targets TRAF family proteins for ubiquitination and degradation. Mol. Cell. Biochem. 338: 11-17.
25. Osmundson EC, Ray D, Moore FE, Gao Q, Thomsen GH, Kiyokawa H. 2008. The HECT E3 ligase Smurf2 is required for Mad2-dependent spindle assembly checkpoint. J. Cell Biol. 183:267-277.
26. Pan W, Choi SC, Wang H, Qin Y, Volpicelli-Daley L, Swan L, Lucast L, Khoo C, Zhang X, Li L, Abrams CS, Sokol SY, Wu D. 2008. Wnt3amediated formation of phosphatidylinositol 4,5-bisphosphate regulates LRP6 phosphorylation. Science 321:1350-1353.
27. Wei W, Li M, Wang J, Nie F, Li L. 2012. The E3 ubiquitin ligase ITCH negatively regulates canonical Wnt signaling by targeting dishevelled protein. Mol. Cell. Biol. 32:3903-3912.
28. Dai J, Jin WH, Sheng QH, Shieh CH, Wu JR, Zeng R. 2007. Protein phosphorylation and expression profiling by Yin-yang multidimensional liquid chromatography (Yin-Yang MDLC) mass spectrometry. J. Proteome Res. 6:250-262.
29. Cox J, Mann M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26:1367-1372.
30. Keshishian H, Addona T, Burgess M, Kuhn E, Carr SA. 2007. Quantitative, multiplexed assays for low abundance proteins in plasma by targeted mass spectrometry and stable isotope dilution. Mol. Cell. Proteomics 6:2212-2229.
31. Suzuki C, Murakami G, Fukuchi M, Shimanuki T, Shikauchi Y, Imamura T, Miyazono K. 2002. Smurf1 regulates the inhibitory activity of Smad7 by targeting Smad7 to the plasma membrane. J. Biol. Chem. 277: 39919-39925.
32. Zeng X, Huang H, Tamai K, Zhang X, Harada Y, Yokota C, Almeida K, Wang J, Doble B, Woodgett J, Wynshaw-Boris A, Hsieh JC, He X. 2008. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development 135:367-375.
33. Hsieh JC, Lee L, Zhang L, Wefer S, Brown K, DeRossi C, Wines ME, Rosenquist T, Holdener BC. 2003. Mesd encodes an LRP5/6 chaperone essential for specification of mouse embryonic polarity. Cell 112:355-367.
34. Yuan C, Qi J, Zhao X, Gao C. 2012. Smurf1 protein negatively regulates interferon-gamma signaling through promoting STAT1 protein ubiquitination and degradation. J. Biol. Chem. 287:17006-17015.
35. Wan L, Zou W, Gao D, Inuzuka H, Fukushima H, Berg AH, Drapp R, Shaik S, Hu D, Lester C, Eguren M, Malumbres M, Glimcher LH, Wei W. 2011. Cdh1 regulates osteoblast function through an APC/Cindependent modulation of Smurf1. Mol. Cell 44:721-733.
36. Cheng PL, Lu H, Shelly M, Gao H, Poo MM. 2011. Phosphorylation of E3 ligase Smurf1 switches its substrate preference in support of axon development. Neuron 69:231-243.
37. Ding Y, Xi Y, Chen T, Wang JY, Tao DL, Wu ZL, Li YP, Li C, Zeng R, Li L. 2008. Caprin-2 enhances canonical Wnt signaling through regulating LRP5/6 phosphorylation. J. Cell Biol. 182:865-872.
38. Wang S, Yin J, Chen D, Nie F, Song X, Fei C, Miao H, Jing C, Ma W, Wang L, Xie S, Li C, Zeng R, Pan W, Hao X, Li L. 2013. Small-molecule modulation of Wnt signaling via modulating the Axin-LRP5/6 interaction. Nat. Chem. Biol. [Epub ahead of print.]
39. Tang N, Song WX, Luo J, Luo X, Chen J, SharffKA, Bi Y, He BC, Huang JY, Zhu GH, Su YX, Jiang W, Tang M, He Y, Wang Y, Chen L, Zuo GW, Shen J, Pan X, Reid RR, Luu HH, Haydon RC, He TC. 2009. BMP-9-induced osteogenic differentiation of mesenchymal progenitors requires functional canonical Wnt/beta-catenin signalling. J. Cell. Mol. Med. 13:2448-2464.
40. Kamiya N, Kobayashi T, Mochida Y, Yu PB, Yamauchi M, Kronenberg HM, Mishina Y. 2010. Wnt inhibitors Dkk1 and Sost are downstream targets of BMP signaling through the type IA receptor (BMPRIA) in osteoblasts. J. Bone Miner. Res. 25:200-210.