Ubiquitin specific protease 4 positively regulates the WNT/β-catenin signaling in colorectal cancer

Molecular Oncology

Volumn 9, Issue 9, 2015, Pages 1834-1851

  Yun, Sun Il ^a   Kim, Hyeon Ho ^b,c   Yoon, Jung Hwan ^d   Park, Won Sang ^d   Hahn, Myong Joon ^a   Kim, Hee Cheol ^a   Chung, Chin Ha ^e   Kim, Kyeong Kyu ^a,b,c  

^a Sungkyunkwan University School of Medicine   (South Korea)

^b Samsung Advanced Institute of Technology (SAIT)   (South Korea)

^c Samsung Medical Center   (South Korea)

^d The Catholic University of Korea   (South Korea)

^e Seoul National University   (South Korea)

Author keywords

Cancer; Ubiquitin specific protease 4 (USP4); catenin

Indexed keywords

BETA CATENIN; DEUBIQUITINASE; UBIQUITIN SPECIFIC PROTEASE 4; UNCLASSIFIED DRUG; WNT PROTEIN; SMALL INTERFERING RNA; UBIQUITIN THIOLESTERASE; USP4 PROTEIN, HUMAN;

ARTICLE; CANCER TISSUE; COLORECTAL CANCER; CONTROLLED STUDY; CORRELATIONAL STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HCT116 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTASIS; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; CELL MOTION; COLON; COLORECTAL TUMOR; GENETICS; METABOLISM; PATHOLOGY; RECTUM; RNA INTERFERENCE; TUMOR INVASION; UBIQUITINATION; WNT SIGNALING PATHWAY;

BETA CATENIN; CELL MOVEMENT; COLON; COLORECTAL NEOPLASMS; HCT116 CELLS; HUMANS; NEOPLASM INVASIVENESS; RECTUM; RNA INTERFERENCE; RNA, SMALL INTERFERING; UBIQUITIN THIOLESTERASE; UBIQUITINATION; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84945484812     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2015.06.006     Document Type: Article

References (43)

1. Anastas J.N., Moon R.T. WNT signaling pathways as therapeutic targets in cancer. Nat. Rev. Cancer 2013, 13:11-26.
2. Baker R.T., Wang X.W., Woollatt E., White J.A., Sutherland G.R. Identification, functional characterization, and chromosomal localization of USP15, a novel human ubiquitin-specific protease related to the UNP oncoprotein, and a systematic nomenclature for human ubiquitin-specific proteases. Genomics 1999, 59:264-274.
3. Bheda A., Yue W., Gullapalli A., Whitehurst C., Liu R., Pagano J.S., Shackelford J. Positive reciprocal regulation of ubiquitin C-terminal hydrolase L1 and beta-catenin/TCF signaling. PLoS One 2009, 4:e5955.
4. Burgess A.W., Faux M.C., Layton M.J., Ramsay R.G. Wnt signaling and colon tumorigenesis - a view from the periphery. Exp. Cell. Res. 2011, 317:2748-2758.
5. Clague M.J., Coulson J.M., Urbé S. Cellular functions of the DUBs. J. Cell. Sci. 2012, 125:277-286.
6. Clerici M., Luna-Vargas M.P., Faesen A.C., Sixma T.K. The DUSP-Ubl domain of USP4 enhances its catalytic efficiency by promoting ubiquitin exchange. Nat. Commun. 2014, 5:5399.
7. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
8. DeSalle L.M., Latres E., Lin D., Graner E., Montagnoli A., Baker R.T., Pagano M., Loda M. The de-ubiquitinating enzyme Unp interacts with the retinoblastoma protein. Oncogene 2001, 20:5538-5542.
9. Fagotto F., Glück U., Gumbiner B.M. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of beta-catenin. Curr. Biol. 1998, 8:181-190.
10. Fan Y.H., Yu Y., Mao R.F., Tan X.J., Xu G.F., Zhang H., Lu X.B., Fu S.B., Yang J. USP4 targets TAK1 to downregulate TNFα-induced NF-κB activation. Cell Death Differ. 2011, 18:1547-1560.
11. Gerard B., Sanders M.A., Visscher D.W., Tait L., Shekhar M.P. Lysine 394 is a novel Rad6B-induced ubiquitination site on beta-catenin. Biochim. Biophys. Acta 2012, 1823:1686-1696.
12. Holland J.D., Klaus A., Garratt A.N., Birchmeier W. Wnt signaling in stem and cancer stem cells. Curr. Opin. Cell Biol. 2013, 25:254-264.
13. Hou X., Wang L., Zhang L., Pan X., Zhao W. Ubiquitin-specific protease 4 promotes TNF-α-induced apoptosis by deubiquitination of RIP1 in head and neck squamous cell carcinoma. FEBS Lett. 2013, 587:311-316.
14. Komiya Y., Habas R. Wnt signal transduction pathways. Organogenesis 2008, 4:68-75.
15. Lee J.R., Chang Y.Y., Hahn M.J. Development of a new epitope tag recognized by a monoclonal antibody to Rickettsia typhi. Biotechniques 2001, 31:541-545.
16. Lee J.T., Gu W. The multiple levels of regulation by p53 ubiquitination. Cell Death Differ. 2010, 17:86-92.
17. Li M., Chen D., Shiloh A., Luo J., Nikolaev A.Y., Qin J., Gu W. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 2002, 416:648-653.
18. Liu W., Dong X., Mai M., Seelan R.S., Taniguchi K., Krishnadath K.K., Halling K.C., Cunningham J.M., Boardman L.A., Qian C., Christensen E., Schmidt S.S., Roche P.C., Smith D.I., Thibodeau S.N. Mutations in AXIN2 cause colorectal cancer with defective mismatch repair by activating beta-catenin/TCF signaling. Nat. Genet. 2000, 26:146-147.
19. Lui T.T., Lacroix C., Ahmed S.M., Goldenberg S.J., Leach C.A., Daulat A.M., Angers S. The ubiquitin-specific protease USP34 regulates axin stability and Wnt/β-catenin signaling. Mol. Cell. Biol. 2011, 31:2053-2065.
20. Luna-Vargas M.P., Faesen A.C., van Dijk W.J., Rape M., Fish A., Sixma T.K. Ubiquitin-specific protease 4 is inhibited by its ubiquitin-like domain. EMBO Rep. 2011, 12:365-372.
21. Milojevic T., Reiterer V., Stefan E., Korkhov V.M., Dorostkar M.M., Ducza E., Ogris E., Boehm S., Freissmuth M., Nanoff C. The ubiquitin-specific protease Usp4 regulates the cell surface level of the A2A receptor. Mol. Pharmacol. 2006, 69:1083-1094.
22. 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.
23. Mukai A., Yamamoto-Hino M., Awano W., Watanabe W., Komada M., Goto S. Balanced ubiquitylation and deubiquitylation of Frizzled regulate cellular responsiveness to Wg/Wnt. EMBO J. 2010, 29:2114-2125.
24. Okochi-Takada E., Nakazawa K., Wakabayashi M., Mori A., Ichimura S., Yasugi T., Ushijima T. Silencing of the UCHL1 gene in human colorectal and ovarian cancers. Int. J. Cancer 2006, 119:1338-1344.
25. Saletta F., Suryo Rahmanto Y., Richardson D.R. The translational regulator eIF3a: the tricky eIF3 subunit. Biochim. Biophys. Acta 2010, 1806:275-286.
26. Sekine S., Shibata T., Sakamoto M., Hirohashi S. Target disruption of the mutant beta-catenin gene in colon cancer cell line HCT116: preservation of its malignant phenotype. Oncogene 2002, 21:5906-5911.
27. Sharma M., Jamieson C., Johnson M., Molloy M.P., Henderson B.R. Specific armadillo repeat sequences facilitate β-catenin nuclear transport in live cells via direct binding to nucleoporins Nup62, Nup153, and RanBP2/Nup358. J. Biol. Chem. 2012, 287:819-831.
28. Soboleva T.A., Jans D.A., Johnson-Saliba M., Baker R.T. Nuclear-cytoplasmic shuttling of the oncogenic mouse UNP/USP4 deubiquitylating enzyme. J. Biol. Chem. 2005, 280:745-752.
29. Song E.J., Werner S.L., Neubauer J., Stegmeier F., Aspden J., Rio D., Harper J.W., Elledge S.J., Kirschner M.W., Rape M. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 2010, 24:1434-1447.
30. Tauriello D.V., Haegebarth A., Kuper I., Edelmann M.J., Henraat M., Canninga-van Dijk M.R., Kessler B.M., Clevers H., Maurice M.M. Loss of the tumor suppressor CYLD enhances Wnt/beta-catenin signaling through K63-linked ubiquitination of Dvl. Mol. Cell 2010, 37:607-619.
31. Taya S., Yamamoto T., Kanai-Azuma M., Wood S.A., Kaibuchi K. The deubiquitinating enzyme Fam interacts with and stabilizes β-catenin. Genes Cells 1999, 4:757-767.
32. Uras I.Z., List T., Nijman S.M. Ubiquitin-specific protease 4 inhibits mono-ubiquitination of the master growth factor signaling kinase PDK1. PLoS One 2012, 7:e31003.
33. Wada K., Kamitani T. Oncogenic protein UnpEL/Usp4 deubiquitinates Ro52 by its isopeptidase activity. Biochem. Biophys. Res. Commun. 2006, 342:253-258.
34. Wang G., Gao Y., Li L., Jin G., Cai Z., Chao J.I., Lin H.K. K63-linked ubiquitination in kinase activation and cancer. Front. Oncol. 2012, 2:5.
35. Wang L., Zhao W., Zhang M., Wang P., Zhao K., Zhao X., Yang S., Gao C. USP4 positively regulates RIG-I-mediated antiviral response through deubiquitination and stabilization of RIG-I. J. Virol. 2013, 87:4507-4515.
36. Watanabe K., Dai X. Winning WNT: race to Wnt signaling inhibitors. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5929-5930.
37. Wu X., Tu X., Joeng K.S., Hilton M.J., Williams D.A., Long F. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 2008, 133:340-353.
38. Xiao N., Li H., Luo J., Wang R., Chen H., Chen J., Wang P. Ubiquitin-specific protease 4 (USP4) targets TRAF2 and TRAF6 for deubiquitination and inhibits TNFα-induced cancer cell migration. Biochem. J. 2012, 441:979-986.
39. Yuan J., Luo K., Zhang L., Cheville J.C., Lou Z. USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 2010, 140:384-396.
40. Zhang X., Berger F.G., Yang J., Lu X. USP4 inhibits p53 through deubiquitinating and stabilizing ARF-BP1. EMBO J. 2011, 30:2177-2189.
41. Zhao B., Schlesiger C., Masucci M.G., Lindsten K. The ubiquitin specific protease 4 (USP4) is a new player in the Wnt signaling pathway. J. Cell. Mol. Med. 2009, 13:1886-1895.
42. Zhao B., Velasco K., Sompallae R., Pfirrmann T., Masucci M.G., Lindsten K. The ubiquitin specific protease-4 (USP4) interacts with the S9/Rpn6 subunit of the proteasome. Biochem. Biophys. Res. Commun. 2012, 427:490-496.
43. Zucker S., Vacirca J. Role of matrix metalloproteinases (MMPs) in colorectal cancer. Cancer Metastasis Rev. 2004, 23:101-117.