The ubiquitin-specific protease USP28 is required for MYC stability

Nature Cell Biology

Volumn 9, Issue 7, 2007, Pages 765-774

  Popov, Nikita ^a   Wanzel, Michael ^a   Madiredjo, Mandy ^b   Zhang, Dong ^c   Beijersbergen, Roderick ^b   Bernards, Rene ^b   Moll, Roland ^a   Elledge, Stephen J ^c   Eilers, Martin ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c LABORATORY FOR MOLECULAR MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F BOX PROTEIN; MUCIN 2; MYC PROTEIN; PROTEIN FBW 7 ALPHA; PROTEINASE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR GAL4; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE 28; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE TARGETING; GENETIC IDENTIFICATION; GENETIC REGULATION; GENETIC SCREENING; HUMAN; HUMAN CELL; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STEM CELL; SUPPRESSOR GENE; UNINDEXED SEQUENCE;

ADENOCARCINOMA; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; CELL NUCLEOLUS; CELL NUCLEUS; CELL PROLIFERATION; COLONIC NEOPLASMS; F-BOX PROTEINS; HUMANS; LIVER NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN THIOLESTERASE;

EID: 34347401998     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1601     Document Type: Article

References (49)

1. Oster, S. K., Ho, C. S., Soucie, E. L. & Penn, L. Z. The myc oncogene: MarvelousIY Complex. Adv. Cancer Res. 84, 81-154 (2002).
2. 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. 18, 717-726 (1999).
3. Bahram, F., von der Lehr, N., Cetinkaya, C. & Larsson, L. G. c-MYC hot spot mutations in lymphomas result in inefficient ubiquitination and decreased proteasome-mediated turnover. Blood 95, 2104-2110 (2000).
4. Welcker, M. et al. The FBW7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-MYC protein degradation. Proc. Natl Acad. Sci. USA 101, 9085-9090 (2004).
5. Yada, M. et al. Phosphorylation-dependent degradation of c-MYC is mediated by the F-box protein FBW7. EMBO J. 23, 2116-2125 (2004).
6. Yeh, E. et al. A signalling pathway controlling c-MYC degradation that impacts oncogenic transformation of human cells. Nature Cell Biol. 6, 308-318 (2004).
7. Gregory, M. A. & Hann, S. R. c-MYC proteolysis by the ubiquitin-proteasome pathway: Stabilization of c-MYC in Burkitt's lymphoma cells. Mol. Cell Biol. 20, 2423-2435 (2000).
8. Malempati, S. et al. Aberrant stabilization of c-MYC protein in some lymphoblastic leukemias. Leukemia 20, 1572-1581 (2006).
9. Kim, S. Y., Herbst, A., Tworkowski, K. A., Salghetti, S. E. & Tansey, W. P. Skp2 regulates myc protein stability and activity. Mol. Cell 11, 1177-1188 (2003).
10. von der Lehr, N. et al. The F-box protein Skp2 participates in c-MYC proteosomal degradation and acts as a cofactor for c-MYC-regulated transcription. Mol. Cell 11, 1189-1200 (2003).
11. Gross-Mesilaty, S. et al. Basal and human papillomavirus E6 oncoprotein-induced degradation of MYC proteins by the ubiquitin pathway. Proc. Natl Acad. Sci. USA 95, 8058-8063 (1998).
12. Nijman, S. M. et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (2005).
13. Evan, G. I. et al. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69, 119-128 (1992).
14. Littlewood, T. D., Hancock, D. C., Danielian, P. S., Parker, M. G. & Evan, G. I. A modified oestrogen receptor ligand binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23, 1686-1690 (1995).
15. Berns, K. et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 428, 431-437 (2004).
16. Brummelkamp, T. R. et al. An shRNA barcode screen provides insight into cancer cell vulnerability to MDM2 inhibitors. Nature Chem. Biol. 2, 202-206 (2006).
17. Amati, B., Littlewood, T. D., Evan, G. I. & Land, H. The c-MYC protein induces cell cycle progression and apoptosis through dimerization with Max. EMBO J. 13, 5083-5087 (1993).
18. Leone, G. et al. MYC requires distinct E2F activities to induce S phase and apoptosis. Mol. Cell 8, 105-113 (2001).
19. Dansen, T. B., Whitfield, J., Rostker, F., Brown-Swigart, L. & Evan, G. I. Specific requirement for Bax, not Bak, in MYC-induced apoptosis and tumor suppression in vivo. J. Biol. Chem. 281, 10890-10895 (2006).
20. Rothermund, K. et al. c-MYC-independent restoration of multiple phenotypes by two c-MYC target genes with overlapping functions. Cancer Res. 65, 2097-2107 (2005).
21. Benitah, S. A., Frye, M., Glogauer, M. & Watt, F. M. Stem cell depletion through epidermal deletion of Rac1. Science 309, 933-935 (2005).
22. Park, Y. B. et al. Alterations in the INK4a/ARF locus and their effects on the growth of human osteosarcoma cell lines. Cancer Genet. Cytogenet. 133, 105-111 (2002).
23. Zhang, D., Zaugg, K., Mak, T. W. & Elledge, S. J. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 126, 529-542 (2006).
24. Koepp, D. M. et al. Phosphorylation-dependent ubiquitination of cyclin E by the SCFFBW7 ubiquitin ligase. Science 294, 173-177 (2001).
25. Strohmaier, H. et al. Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413, 316-322 (2001).
26. Bhattacharya, S. et al. SKP2 associates with p130 and accelerates p130 ubiquitylation and degradation in human cells. Oncogene 22 2443-2451 (2003).
27. Sutterlüty, H. et al. p45skp2 promotes p27kip1 degradation and induces S phase in quiescent cells. Nature Cell Biol. 1, 207-214 (1999).
28. Sorensen, C. S. et al. A conserved cyclin-binding domain determines functional interplay between anaphase-promoting complex-Cdh1 and cyclin A-Cdk2 during cell cycle progression. Mol. Cell Biol. 21, 3692-3703 (2001).
29. Bashir, T., Dorrello, N. V., Amador, V., Guardavaccaro, D. & Pagano, M. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428, 190-193 (2004).
30. Welcker, M. et al. Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation. Mol. Cell 12, 381-392 (2003).
31. Welcker, M., Orian, A., Grim, J. A., Eisenman, R. N. & Clurman, B. E. A Nucleolar isoform of the FBW7 ubiquitin ligase regulates c-MYC and cell size. Curr. Biol. 14, 1852-1857 (2004).
32. Kee, Y., Lyon, N. & Huibregtse, J. M. The Rsp5 ubiquitin ligase is coupled to and antagonized by the Ubp2 deubiquitinating enzyme. EMBO J. 24, 2414-2424 (2005).
33. Li, M., Brooks, C. L., Kon, N. & Gu, W. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell 13, 879-886 (2004).
34. van Drogen, F. et al. Ubiquitylation of cyclin E requires the sequential function of SCF complexes containing distinct hCdc4 isoforms. Mol. Cell 23, 37-48 (2006).
35. Gomez-Roman, N., Grandori, C., Eisenman, R. N. & White, R. J. Direct activation of RNA polymerase III transcription by c-MYC. Nature 421, 290-294 (2003).
36. Grandori, C. et al. c-MYC binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nature Cell Biol. 7, 311-318 (2005).
37. Sansom, O. J. et al. MYC deletion rescues Apc deficiency in the small intestine. Nature 446, 676-679 (2007).
38. van de Wetering, M. et al. The β-catenin/CF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111 241-250 (2002).
39. Oskarsson, T. & Trumpp, A. The MYC trilogy: Lord of RNA polymerases. Nature Cell Biol. 7, 215-217 (2005).
40. Arabi, A., Rustum, C., Hallberg, E. & Wright, A. P. Accumulation of c-MYC and proteasomes at the nucleoli of cells containing elevated c-MYC protein levels. J. Cell Sci. 116, 1707-1717 (2003).
41. Li, Z., Wang, D., Messing, E. M. & Wu, G. VHL protein-interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF-1α. EMBO Rep. 6, 373-378 (2005).
42. Herbst, A. et al. A conserved element in MYC that negatively regulates its proapoptotic activity. EMBO Rep. 6, 177-183 (2005).
43. Hemann, M. T. et al. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 436, 807-811 (2005).
44. Benassi, B. et al. c-MYC phosphorylation is required for cellular response to oxidative stress. Mol. Cell 21, 509-519 (2006).
45. Ngo, V. N. et al. A loss-of-function RNA interference screen for molecular targets in cancer. Nature 441, 106-110 (2006).
46. Shachaf, C. M. et al. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 431, 1112-1117 (2004).
47. Leung-Toung, R. et al. Thiol proteases: Inhibitors and potential therapeutic targets. Curr. Med. Chem. 13, 547-581 (2006).
48. Brummelkamp, T. R., Bernards, R. & Agami, R. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2, 243-247 (2002).
49. Adhikary, S. et al. The ubiquitin ligase HectH9 regulates transcriptional activation by MYC and is essential for tumor cell proliferation. Cell 123, 409-421 (2005).