The Wnt signaling antagonist dapper1 accelerates dishevelled2 degradation via promoting its ubiquitination and aggregate-induced autophagy

Journal of Biological Chemistry

Volumn 290, Issue 19, 2015, Pages 12346-12354

  Ma, Benyu ^a   Liu, Bofeng ^a   Cao, Weipeng ^a   Gao, Chan ^a,b   Qi, Zhen ^a   Ning, Yuanhengk ^a   Chen, Ye Guang ^a  

^a Peking University   (China)

^b Genomic Institute of the Novetis Foundation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; ENZYME INHIBITION; PROTEINS;

AGGREGATED PROTEIN; AUTOPHAGIC DEGRADATION; AUTOPHAGOSOMES; PROTEIN AGGREGATES; TUMOR SUPPRESSORS; UBIQUITINATION; VON HIPPEL LINDAU; WNT SIGNALING;

AGGREGATES;

ATG14L PROTEIN; BECLIN 1; BINDING PROTEIN; DAPPER1; DISHEVELLED 2; HUNTINGTIN; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; PROTEIN P62; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN; DACT1 PROTEIN, HUMAN; DACT1 PROTEIN, RAT; DISHEVELLED PROTEINS; FRODO PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; UBIQUITIN; VHL PROTEIN, HUMAN; VHLH PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; COMPLEX FORMATION; CONTROLLED STUDY; DPR1 GENE; EMBRYO; ENZYME ACTIVITY; GENE SILENCING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; WNT SIGNALING PATHWAY; ANIMAL; CELL LINE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HUMAN; LYSOSOME; METABOLISM; MUTATION; PLASMID; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; CELL LINE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; MICE; MICROSCOPY, FLUORESCENCE; MUTATION; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PLASMIDS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RATS; UBIQUITIN; UBIQUITINATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN; WNT SIGNALING PATHWAY;

EID: 84929103686     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.654590     Document Type: Article

References (42)

1. Shibutani, S. T., and Yoshimori, T. (2014) A current perspective of autophagosome biogenesis. Cell Res. 24, 58-68
2. Hurley, J. H., and Schulman, B. A. (2014) Atomistic autophagy: the structures of cellular self-digestion. Cell 157, 300-311
3. Feng, Y., He, D., Yao, Z., and Klionsky, D. J. (2014) The machinery of macroautophagy. Cell Res. 24, 24-41
4. Mizushima, N., Yoshimori, T., and Ohsumi, Y. (2011) The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132
5. Mizushima, N., and Komatsu, M. (2011) Autophagy: renovation of cells and tissues. Cell 147, 728-741
6. Dall'Armi, C., Devereaux, K. A., and Di Paolo, G. (2013) The role of lipids in the control of autophagy. Curr. Biol. 23, R33-R45
7. Kraft, C., and Martens, S. (2012) Mechanisms and regulation of autophagosome formation. Curr. Opin. Cell Biol. 24, 496-501
8. Lamark, T., and Johansen, T. (2012) Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int. J. Cell Biol. 2012, 736905
9. Lamark, T., Kirkin, V., Dikic, I., and Johansen, T. (2009) NBR1 and p62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 8, 1986-1990
10. Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Øvervatn, A., Bjørkøy, G., and Johansen, T. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145
11. Filimonenko, M., Isakson, P., Finley, K. D., Anderson, M., Jeong, H., Melia, T. J., Bartlett, B. J., Myers, K. M., Birkeland, H. C., Lamark, T., Krainc, D., Brech, A., Stenmark, H., Simonsen, A., and Yamamoto, A. (2010) The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol. Cell 38, 265-279
12. Wong, E., Bejarano, E., Rakshit, M., Lee, K., Hanson, H. H., Zaarur, N., Phillips, G. R., Sherman, M. Y., and Cuervo, A. M. (2012) Molecular determinants of selective clearance of protein inclusions by autophagy. Nat. Commun. 3, 1240
13. Anastas, J. N., and Moon, R. T. (2013) WNT signalling pathways as therapeutic targets in cancer. Nat. Rev. Cancer 13, 11-26
14. Clevers, H., and Nusse, R. (2012) Wnt/β-catenin signaling and disease. Cell 149, 1192-1205
15. Gao, C., Cao, W., Bao, L., Zuo, W., Xie, G., Cai, T., Fu, W., Zhang, J., Wu, W., Zhang, X., and Chen, Y. G. (2010) Autophagy negatively regulates Wnt signalling by promoting Dishevelled degradation. Nat. Cell Biol. 12, 781-790
16. Cheyette, B. N., Waxman, J. S., Miller, J. R., Takemaru, K., Sheldahl, L. C., Khlebtsova, N., Fox, E. P., Earnest, T., and Moon, R. T. (2002) Dapper, a Dishevelled-associated antagonist of β-catenin and JNK signaling, is required for notochord formation. Dev. Cell 2, 449-461
17. Chen, H., Liu, L., Ma, B., Ma, T. M., Hou, J. J., Xie, G. M., Wu, W., Yang, F. Q., and Chen, Y. G. (2011) Protein kinase A-mediated 14-3-3 association impedes human Dapper1 to promote dishevelled degradation. J. Biol. Chem. 286, 14870-14880
18. Wen, J., Chiang, Y. J., Gao, C., Xue, H., Xu, J., Ning, Y., Hodes, R. J., Gao, X., and Chen, Y. G. (2010) Loss of Dact1 disrupts planar cell polarity signaling by altering dishevelled activity and leads to posterior malformation in mice. J. Biol. Chem. 285, 11023-11030
19. Zhang, L., Gao, X., Wen, J., Ning, Y., and Chen, Y. G. (2006) Dapper 1 antagonizes Wnt signaling by promoting dishevelled degradation. J. Biol. Chem. 281, 8607-8612
20. Ma, B., Cao, W., Li, W., Gao, C., Qi, Z., Zhao, Y., Du, J., Xue, H., Peng, J., Wen, J., Chen, H., Ning, Y., Huang, L., Zhang, H., Gao, X., et al. (2014) Dapper1 promotes autophagy by enhancing the Beclin1-Vps34-Atg14L complex formation. Cell Res. 24, 912-924
21. Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J. A., Ahn, H. J., Ait-Mohamed, O., Ait-Si-Ali, S., Akematsu, T., Akira, S., et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445-544
22. Mizushima, N., Yoshimori, T., and Levine, B. (2010) Methods in mammalian autophagy research. Cell 140, 313-326
23. Kaelin, W. G. (2005) The von Hippel-Lindau tumor suppressor protein: roles in cancer and oxygen sensing. Cold Spring Harb. Symp. Quant. Biol. 70, 159-166
24. Schwarz-Romond, T., Fiedler, M., Shibata, N., Butler, P. J., Kikuchi, A., Higuchi, Y., and Bienz, M. (2007) The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat. Struct. Mol. Biol. 14, 484-492
25. Schwarz-Romond, T., Merrifield, C., Nichols, B. J., and Bienz, M. (2005) The Wnt signalling effector Dishevelled forms dynamic protein assemblies rather than stable associations with cytoplasmic vesicles. J. Cell Sci. 118, 5269-5277
26. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H., and Johansen, T. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171, 603-614
27. Yamamoto, A., Cremona, M. L., and Rothman, J. E. (2006) Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway. J. Cell Biol. 172, 719-731
28. Itakura, E., and Mizushima, N. (2011) p62 targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J. Cell Biol. 192, 17-27
29. Pashkova, N., Gakhar, L., Winistorfer, S. C., Yu, L., Ramaswamy, S., and Piper, R. C. (2010) WD40 repeat propellers define a ubiquitin-binding domain that regulates turnover of F box proteins. Mol. Cell 40, 433-443
30. Fujita, N., Morita, E., Itoh, T., Tanaka, A., Nakaoka, M., Osada, Y., Umemoto, T., Saitoh, T., Nakatogawa, H., Kobayashi, S., Haraguchi, T., Guan, J. L., Iwai, K., Tokunaga, F., Saito, K., et al. (2013) Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 203, 115-128
31. Chaari, A., Hoarau-Véchot, J., and Ladjimi, M. (2013) Applying chaperones to protein-misfolding disorders: molecular chaperones against α-synuclein in Parkinson's disease. Int. J. Biol. Macromol. 60, 196-205
32. Yang, Y., Fiskus, W., Yong, B., Atadja, P., Takahashi, Y., Pandita, T. K., Wang, H. G., and Bhalla, K. N. (2013) Acetylated hsp70 and KAP1-mediated Vps34 SUMOylation is required for autophagosome creation in autophagy. Proc. Natl. Acad. Sci. U.S.A. 110, 6841-6846
33. Kirkin, V., McEwan, D. G., Novak, I., and Dikic, I. (2009) A role for ubiquitin in selective autophagy. Mol. Cell 34, 259-269
34. Rogov, V., Dötsch, V., Johansen, T., and Kirkin, V. (2014) Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol. Cell 53, 167-178
35. Yang, Y., Kitagaki, J., Dai, R. M., Tsai, Y. C., Lorick, K. L., Ludwig, R. L., Pierre, S. A., Jensen, J. P., Davydov, I. V., Oberoi, P., Li, C. C., Kenten, J. H., Beutler, J. A., Vousden, K. H., and Weissman, A. M. (2007) Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res. 67, 9472-9481
36. Gao, C., and Chen, Y. G. (2010) Dishevelled: The hub of Wnt signaling. Cell. Signal. 22, 717-727
37. Ding, Y., Zhang, Y., Xu, C., Tao, Q. H., and Chen, Y. G. (2013) HECT domain-containing E3 ubiquitin ligase NEDD4L negatively regulates Wnt signaling by targeting dishevelled for proteasomal degradation. J. Biol. Chem. 288, 8289-8298
38. Suriben, R., Kivimäe, S., Fisher, D. A., Moon, R. T., and Cheyette, B. N. (2009) Posterior malformations in Dact1 mutant mice arise through misregulated Vangl2 at the primitive streak. Nat. Genet. 41, 977-985
39. Jiang, P., and Mizushima, N. (2014) Autophagy and human diseases. Cell Res. 24, 69-79
40. Svenning, S., and Johansen, T. (2013) Selective autophagy. Essays Biochem. 55, 79-92
41. Rubinsztein, D. C., Mariño, G., and Kroemer, G. (2011) Autophagy and aging. Cell 146, 682-695
42. Korac, J., Schaeffer, V., Kovacevic, I., Clement, A. M., Jungblut, B., Behl, C., Terzic, J., and Dikic, I. (2013) Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J. Cell Sci. 126, 580-592