USP4 is regulated by AKT phosphorylation and directly deubiquitylates TGF-β type i receptor

Nature Cell Biology

Volumn 14, Issue 7, 2012, Pages 717-726

  Zhang, Long ^a   Zhou, Fangfang ^a   Drabsch, Yvette ^a   Gao, Rui ^b   Snaar Jagalska, B Ewa ^c   Mickanin, Craig ^d   Huang, Huizhe ^e   Sheppard, Kelly Ann ^d   Porter, Jeff A ^d   Lu, Chris X ^d   Ten Dijke, Peter ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b XIAMEN UNIVERSITY   (China)

^c LEIDEN UNIVERSITY   (Netherlands)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; MESSENGER RNA; PROTEIN KINASE B; PROTEINASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UBIQUITIN SPECIFIC PROTEASE 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INVASION; CANCER PROGNOSIS; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM VESICLE; DISEASE ASSOCIATION; EMBRYO; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; METASTASIS; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TUMOR GENE; UBIQUITIN SPECIFIC PROTEASE 4 GENE; UBIQUITINATION;

ANIMALS; BREAST NEOPLASMS; CELL MEMBRANE; CELL MOVEMENT; ENZYME STABILITY; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; MUTATION; NEOPLASM INVASIVENESS; ONCOGENE PROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN THIOLESTERASE; UBIQUITINATION; ZEBRAFISH;

EID: 84863218422     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2522     Document Type: Article

References (59)

1. Moustakas, A. & Heldin, C. H. The regulation of TGfisignal transduction. Development 136, 3699-3714 (2009).
2. Kang, J. S., Liu, C. & Derynck, R. New regulatory mechanisms of TGfireceptor function. Trends Cell Biol. 19, 385-394 (2009).
3. Ikushima, H. & Miyazono, K. TGfisignalling: a complex web in cancer progression. Nat. Rev. Cancer 10, 415-424 (2010).
4. Massague, J. TGfiin cancer. Cell 134, 215-230 (2008).
5. Bakin, A. V., Tomlinson, A. K., Bhowmick, N. A., Moses, H. L. & Arteaga, C. L. Phosphatidylinositol 3-kinase function is required for transforming growth factor-mediated epithelial to mesenchymal transition and cell migration. J. Biol. Chem. 275, 36803-36810 (2000). (Pubitemid 32002090)
6. Muraoka, R. S. et al. Blockade of TGfiinhibits mammary tumor cell viability, migration, and metastases. J. Clin. Invest. 109, 1551-1559 (2002). (Pubitemid 34663517)
7. Brown, R.L. et al. CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J. Clin. Invest. 121, 1064-1074 (2011).
8. Lamouille, S., Connolly, E., Smyth, J. W., Akhurst, R. J. & Derynck, R. TGfi-induced activation of mTOR complex 2 drives epithelial-mesenchymal transition and cell invasion. J. Cell Sci. 125, 1259-1273 (2012).
9. Pollak, M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat. Rev. Cancer 12, 159-169 (2012).
10. Pietenpol, J. A. et al. TGfi1 Inhibition of C-Myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRb binding domains. Cell 61, 777-785 (1990).
11. Adorno, M. et al. A Mutant-p53/SMAD complex opposes p63 to empower TGfiinduced metastasis. Cell 137, 87-98 (2009).
12. Oft, M. et al. TGfi1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev. 10, 2462-2477 (1996). (Pubitemid 26341881)
13. Smith, A. P. et al. A positive role for Myc in TGfiinduced Snail transcription and epithelial-to-mesenchymal transition. Oncogene 28, 422-430 (2009).
14. Zhang, Y. E. Non-SMAD pathways in TGfisignaling. Cell Res. 19, 128-139 (2009).
15. Muraoka-Cook, R. S. et al. Activated type I TGfireceptor kinase enhances the survival of mammary epithelial cells and accelerates tumor progression. Oncogene 25, 3408-3423 (2006). (Pubitemid 43877044)
16. Parvani, J. G., Taylor, M. A. & Schiemann, W. P. Noncanonical TGfisignaling during mammary tumorigenesis. J. Mammary Gland Biol. Neoplasia 16, 127-146 (2011).
17. Lonn, P., Moren, A., Raja, E., Dahl, M. & Moustakas, A. Regulating the stability of TGfireceptors and SMADs. Cell Res. 19, 21-35 (2009).
18. De Boeck, M. & ten Dijke, P. Key role for ubiquitin protein modi-cation in TGfisignal transduction. Ups J. Med. Sci. 117, 153-165 (2012).
19. Zhu, H., Kavsak, P., Abdollah, S., Wrana, J. L. & Thomsen, G. H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400, 687-693 (1999).
20. Lin, X., Liang, M. & Feng, X. H. SMURF2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of SMAD2 in transforming growth factor-signaling. J. Biol. Chem. 275, 36818-36822 (2000). (Pubitemid 32002092)
21. Zhang, Y., Chang, C. B., Gehling, D. J., Hemmati-Brivanlou, A. & Delynck, R. Regulation of SMAD degradation and activity by SMURF2, an E3 ubiquitin ligase. Proc. Natl Acad. Sci. USA 98, 974-979 (2001). (Pubitemid 32121172)
22. Lo, R. S. & Massague, J. Ubiquitin-dependent degradation of TGfi-activated SMAD2. Nat. Cell Biol. 1, 472-478 (1999).
23. Nijman, S. M. B. et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (2005). (Pubitemid 41721026)
24. Yuan, J., Luo, K. T., Zhang, L. Z., Cheville, J. C. & Lou, Z. K. USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 140, 384-U121 (2010).
25. Williams, S. A. et al. USP1 deubiquitinates ID proteins to preserve a mesenchymal stem cell program in osteosarcoma. Cell 146, 917-929 (2011).
26. Nakada, S. et al. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466, 941-U959 (2010).
27. Inui, M. et al. USP15 is a deubiquitylating enzyme for receptor-activated SMADs. Nat. Cell Biol. 13, 1368-U1187 (2011).
28. Kavsak, P. et al. SMAD7 binds to SMURF2 to form an E3 ubiquitin ligase that targets the TGfireceptor for degradation. Molecular Cell. 6, 1365-1375 (2000). (Pubitemid 32045929)
29. Suzuki, C. et al. SMURF1 regulates the inhibitory activity of SMAD7 by targeting SMAD7 to the plasma membrane. J. Biol. Chem. 277, 39919-39925 (2002). (Pubitemid 35190978)
30. Eichhorn, P. J. et al. USP15 stabilizes TGfireceptor I and promotes oncogenesis through the activation of TGfisignaling in glioblastoma. Nat. Med. 18, 429-435 (2012).
31. Zhou, F. et al. Ubiquitin-speci-c protease 4 mitigates Toll-like/interleukin-1 receptor signaling and regulates innate immune activation. J. Biol. Chem. 287, 11002-11010 (2012).
32. Guglielmo, G. M. Distinct endocytic pathways regulate TGfireceptor signalling and turnover. Nat. Cell Biol. 5, 410-421 (2003). (Pubitemid 36592263)
33. Zhang, X. N., Berger, F. G., Yang, J. H. & Lu, X. B. USP4 inhibits p53 through deubiquitinating and stabilizing ARfiBP1. EMBO J. 30, 2177-2189 (2011).
34. Xu, J., Lamouille, S. & Derynck, R. TGfi-induced epithelial to mesenchymal transition. Cell Res. 19, 156-172 (2009).
35. Thiery, J. P., Acloque, H., Huang, R. Y. & Nieto, M. A. Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890 (2009).
36. He, S. et al. Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebra-sh xenograft model. J. Pathol. http://dx.doi.org/10. 1002/path. 4013 (2012).
37. Kang, Y. B. et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (2003).
38. Bandyopadhyay, A. et al. Inhibition of pulmonary and skeletal metastasis by a transforming growth factor-type I receptor kinase inhibitor. Cancer Res. 66, 6714-6721 (2006). (Pubitemid 44085629)
39. Manning, B. D. & Cantley, L. C. AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274 (2007). (Pubitemid 46962095)
40. Tran, H., Brunet, A., Grifith, E. C. & Greenberg, M. E. The many forks in FOXO's road. Sci STKE 2003, RE5 (2003).
41. Freeman, A. K. & Morrison, D. K. 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin. Cell Dev. Biol. 22, 681-687 (2011).
42. Wada, K. & Kamitani, T. UnpEL/Usp4 is ubiquitinated by Ro52 and deubiquitinated by itself. Biochem. Biophys. Res. Commun. 342, 253-258 (2006). (Pubitemid 43247384)
43. Sowa, M. E., Bennett, E. J., Gygi, S. P. & Harper, J. W. De-ning the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403 (2009).
44. Fan, Y. H. et al. USP4 targets TAK1 to downregulate TNfiinduced NfiB activation. Cell Death Differ. 18, 1547-1560 (2011).
45. Xiao, N. et al. Ubiquitin-speci-c protease 4 (USP4) targets TRAF2 and TRAF6 for deubiquitination and inhibits TNfiinduced cancer cell migration. Biochem. J. 441, 979-986 (2012).
46. Inui, M. et al. USP15 is a deubiquitylating enzyme for receptor-activated SMADs. Nat. Cell Biol. 13, 1368-1375 (2011).
47. Conery, A. R. et al. AKT interacts directly with SMAD3 to regulate the sensitivity to TGfi-induced apoptosis. Nat. Cell Biol. 6, 366-372 (2004). (Pubitemid 38584827)
48. Remy, I., Montmarquette, A. & Michnick, S. W. PKB/AKT modulates TGfisignalling through a direct interaction with SMAD3. Nat. Cell Biol. 6, 358-365 (2004). (Pubitemid 38584826)
49. Daly, A. C., Vizan, P. & Hill, C. S. SMAD3 protein levels are modulated by Ras activity and during the cell cycle to dictate transforming growth factor-responses. J. Biol. Chem. 285, 6489-6497 (2009).
50. Han, S. U. et al. Loss of the SMAD3 expression increases susceptibility to tumorigenicity in human gastric cancer. Oncogene 23, 1333-1341 (2004).
51. Cohen, P. & Tcherpakov, M. Will the ubiquitin system furnish as many drug targets as protein kinases? Cell 143, 686-693 (2010).
52. Strausberg, R. L., Feingold, E. A., Klausner, R. D. & Collins, F. S. The mammalian gene collection. Science 286, 455-457 (1999).
53. Cao, Y., Zhao, J., Sun, Z. H., Postlethwait, J. & Meng, A. M. fgf17b, a novel member of Fgf family, helps patterning zebra-sh embryos. Dev. Biol. 271, 130-143 (2004). (Pubitemid 38757781)
54. Zhang, L. X. et al. Zebra-sh Dpr2 inhibits mesoderm induction by promoting degradation of nodal receptors. Science 306, 114-117 (2004).
55. Prince, V. E., Price, A. L. & Ho, R. K. Hox gene expression reveals regionalization along the anteroposterior axis of the zebra-sh notochord. Dev. Genes Evol. 208, 517-522 (1998). (Pubitemid 28505325)
56. White, R. M. et al. Transparent adult zebra-sh as a tool for in vivo transplantation analysis. Cell Stem Cell 2, 183-189 (2008). (Pubitemid 351168711)
57. Lee, L. M. J., Seftor, E. A., Bonde, G., Cornell, R. A. & Hendrix, M. J. C. The fate of human malignant melanoma cells transplanted into zebra-sh embryos: assessment of migration and cell division in the absence of tumor formation. Dev. Dynam. 233, 1560-1570 (2005). (Pubitemid 40995154)
58. Nakao, A. et al. Identi-cation of SMAD7, a TGfiinducible antagonist of TGfisignalling. Nature 389, 631-635 (1997).
59. Zhang, L. et al. Fas-associated factor 1 antagonizes Wnt signaling by promoting beta-catenin degradation. Mol. Biol. Cell 22, 1617-1624 (2011).