XIAP Monoubiquitylates Groucho/TLE to Promote Canonical Wnt Signaling

Molecular Cell

Volumn 45, Issue 5, 2012, Pages 619-628

  Hanson, Alison J ^a   Wallace, Heather A ^a   Freeman, Tanner J ^a,b   Beauchamp, R Daniel ^a,b,c   Lee, Laura A ^a,c   Lee, Ethan ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DROSOPHILA INHIBITOR OF APOPTOSIS 1; INHIBITOR OF APOPTOSIS PROTEIN 1; UNCLASSIFIED DRUG; WNT PROTEIN; X LINKED INHIBITOR OF APOPTOSIS;

ARTICLE; DROSOPHILA; EMBRYO; NONHUMAN; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION; UBIQUITINATION; XENOPUS;

ANIMALS; CO-REPRESSOR PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; HEK293 CELLS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MODELS, GENETIC; RNA INTERFERENCE; UBIQUITINATION; WNT PROTEINS; WNT SIGNALING PATHWAY; WNT1 PROTEIN; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN; XENOPUS; XENOPUS PROTEINS;

MAMMALIA; VERTEBRATA;

EID: 84858081501     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.12.032     Document Type: Article

References (41)

1. Angers S., Thorpe C.J., Biechele T.L., Goldenberg S.J., Zheng N., MacCoss M.J., Moon R.T. The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-beta-catenin pathway by targeting Dishevelled for degradation. Nat. Cell Biol. 2006, 8:348-357.
2. Barolo S., Stone T., Bang A.G., Posakony J.W. Default repression and Notch signaling: Hairless acts as an adaptor to recruit the corepressors Groucho and dCtBP to Suppressor of Hairless. Genes Dev. 2002, 16:1964-1976.
3. Bergmann A., Steller H. Apoptosis, stem cells, and tissue regeneration. Sci. Signal. 2010, 3:re8.
4. Burstein E., Ganesh L., Dick R.D., van De Sluis B., Wilkinson J.C., Klomp L.W., Wijmenga C., Brewer G.J., Nabel G.J., Duckett C.S. A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J. 2004, 23:244-254.
5. Buscarlet M., Stifani S. The 'Marx' of Groucho on development and disease. Trends Cell Biol. 2007, 17:353-361.
6. Cavallo R.A., Cox R.T., Moline M.M., Roose J., Polevoy G.A., Clevers H., Peifer M., Bejsovec A. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 1998, 395:604-608.
7. Chen S., Guttridge D.C., You Z., Zhang Z., Fribley A., Mayo M.W., Kitajewski J., Wang C.Y. Wnt-1 signaling inhibits apoptosis by activating beta-catenin/T cell factor-mediated transcription. J. Cell Biol. 2001, 152:87-96.
8. Daniels D.L., Weis W.I. Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat. Struct. Mol. Biol. 2005, 12:364-371.
9. Dupont S., Mamidi A., Cordenonsi M., Montagner M., Zacchigna L., Adorno M., Martello G., Stinchfield M.J., Soligo S., Morsut L., et al. FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 2009, 136:123-135.
10. Galbán S., Duckett C.S. XIAP as a ubiquitin ligase in cellular signaling. Cell Death Differ. 2010, 17:54-60.
11. Gasperowicz M., Otto F. Mammalian Groucho homologs: redundancy or specificity?. J. Cell. Biochem. 2005, 95:670-687.
12. Goentoro L., Kirschner M.W. Evidence that fold-change, and not absolute level, of beta-catenin dictates Wnt signaling. Mol. Cell 2009, 36:872-884.
13. Harlin H., Reffey S.B., Duckett C.S., Lindsten T., Thompson C.B. Characterization of XIAP-deficient mice. Mol. Cell. Biol. 2001, 21:3604-3608.
14. Heasman J. Patterning the early Xenopus embryo. Development 2006, 133:1205-1217.
15. Huang Y., Rich R.L., Myszka D.G., Wu H. Requirement of both the second and third BIR domains for the relief of X-linked inhibitor of apoptosis protein (XIAP)-mediated caspase inhibition by Smac. J. Biol. Chem. 2003, 278:49517-49522.
16. Jennings B.H., Ish-Horowicz D. The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 2008, 9:205.
17. Jennings B.H., Pickles L.M., Wainwright S.M., Roe S.M., Pearl L.H., Ish-Horowicz D. Molecular recognition of transcriptional repressor motifs by the WD domain of the Groucho/TLE corepressor. Mol. Cell 2006, 22:645-655.
18. Jiang J., Struhl G. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 1998, 391:493-496.
19. Kao K.R., Elinson R.P. The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol. 1988, 127:64-77.
20. Korinek V., Barker N., Morin P.J., van Wichen D., de Weger R., Kinzler K.W., Vogelstein B., Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 1997, 275:1784-1787.
21. Kuo D., Nie M., De Hoff P., Chambers M., Phillips M., Hirsch A.M., Courey A.J. A SUMO-Groucho Q domain fusion protein: characterization and in vivo Ulp1-mediated cleavage. Protein Expr. Purif. 2011, 76:65-71.
22. LaCasse E.C., Mahoney D.J., Cheung H.H., Plenchette S., Baird S., Korneluk R.G. IAP-targeted therapies for cancer. Oncogene 2008, 27:6252-6275.
23. Lewis J., Burstein E., Reffey S.B., Bratton S.B., Roberts A.B., Duckett C.S. Uncoupling of the signaling and caspase-inhibitory properties of X-linked inhibitor of apoptosis. J. Biol. Chem. 2004, 279:9023-9029.
24. Li M., Brooks C.L., Wu-Baer F., Chen D., Baer R., Gu W. Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science 2003, 302:1972-1975.
25. Liston P., Fong W.G., Kelly N.L., Toji S., Miyazaki T., Conte D., Tamai K., Craig C.G., McBurney M.W., Korneluk R.G. Identification of XAF1 as an antagonist of XIAP anti-Caspase activity. Nat. Cell Biol. 2001, 3:128-133.
26. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
27. Marikawa Y., Elinson R.P. beta-TrCP is a negative regulator of Wnt/beta-catenin signaling pathway and dorsal axis formation in Xenopus embryos. Mech. Dev. 1998, 77:75-80.
28. McMahon A.P., Moon R.T. Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 1989, 58:1075-1084.
29. Minoguchi S., Taniguchi Y., Kato H., Okazaki T., Strobl L.J., Zimber-Strobl U., Bornkamm G.W., Honjo T. RBP-L, a transcription factor related to RBP-Jkappa. Mol. Cell. Biol. 1997, 17:2679-2687.
30. Morin P.J., Sparks A.B., Korinek V., Barker N., Clevers H., Vogelstein B., Kinzler K.W. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275:1787-1790.
31. Perissi V., Jepsen K., Glass C.K., Rosenfeld M.G. Deconstructing repression: evolving models of co-repressor action. Nat. Rev. Genet. 2010, 11:109-123.
32. Roose J., Molenaar M., Peterson J., Hurenkamp J., Brantjes H., Moerer P., van de Wetering M., Destrée O., Clevers H. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 1998, 395:608-612.
33. Russell J.C., Whiting H., Szuflita N., Hossain M.A. Nuclear translocation of X-linked inhibitor of apoptosis (XIAP) determines cell fate after hypoxia ischemia in neonatal brain. J. Neurochem. 2008, 106:1357-1370.
34. Salghetti S.E., Kim S.Y., Tansey W.P. Destruction of Myc by ubiquitin-mediated proteolysis: cancer-associated and transforming mutations stabilize Myc. EMBO J. 1999, 18:717-726.
35. Sierra J., Yoshida T., Joazeiro C.A., Jones K.A. The APC tumor suppressor counteracts beta-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev. 2006, 20:586-600.
36. Srinivasula S.M., Ashwell J.D. IAPs: what's in a name?. Mol. Cell 2008, 30:123-135.
37. Thorne C.A., Hanson A.J., Schneider J., Tahinci E., Orton D., Cselenyi C.S., Jernigan K.K., Meyers K.C., Hang B.I., Waterson A.G., et al. Small-molecule inhibition of Wnt signaling through activation of casein kinase 1α. Nat. Chem. Biol. 2010, 6:829-836.
38. van der Horst A., de Vries-Smits A.M., Brenkman A.B., van Triest M.H., van den Broek N., Colland F., Maurice M.M., Burgering B.M. FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat. Cell Biol. 2006, 8:1064-1073.
39. Wang X.H., Sun X., Meng X.W., Lv Z.W., Du Y.J., Zhu Y., Chen J., Kong D.X., Jin S.Z. beta-catenin siRNA regulation of apoptosis- and angiogenesis-related gene expression in hepatocellular carcinoma cells: potential uses for gene therapy. Oncol. Rep. 2010, 24:1093-1099.
40. Xu Q., Wang Y., Dabdoub A., Smallwood P.M., Williams J., Woods C., Kelley M.W., Jiang L., Tasman W., Zhang K., Nathans J. Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell 2004, 116:883-895.
41. Yamaguchi K., Nagai S., Ninomiya-Tsuji J., Nishita M., Tamai K., Irie K., Ueno N., Nishida E., Shibuya H., Matsumoto K. XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. EMBO J. 1999, 18:179-187.