Nucleolar targeting of the Fbw7 ubiquitin ligase by a pseudosubstrate and glycogen synthase kinase 3

Molecular and Cellular Biology

Volumn 31, Issue 6, 2011, Pages 1214-1224

  Welcker, Markus ^a   Larimore, Elizabeth A ^a,c   Frappier, Lori ^d   Clurman, Bruce E ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EPSTEIN BARR VIRUS ANTIGEN 1; F BOX PROTEIN; GLYCOGEN SYNTHASE KINASE 3; PROTEIN FBW7; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; MUTATION; NUCLEOLAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN TARGETING;

CARRIER PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL NUCLEOLUS; CELLS, CULTURED; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MUTATION; NEOPLASMS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN TRANSPORT; SKP CULLIN F-BOX PROTEIN LIGASES;

EID: 79952260898     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01347-10     Document Type: Article

References (55)

1. Akhoondi, S., et al. 2007. FBXW7/hCDC4 is a general tumor suppressor in human cancer. Cancer Res. 67:9006-9012. (Pubitemid 47535882)
2. Amin, M. A., S. Matsunaga, S. Uchiyama, and K. Fukui. 2008. Depletion of nucleophosmin leads to distortion of nucleolar and nuclear structures in HeLa cells. Biochem. J. 415:345-351.
3. Bonetti, P., et al. 2008. Nucleophosmin and its AML-associated mutant regulate c-Myc turnover through Fbw7 gamma. J. Cell Biol. 182:19-26. (Pubitemid 352008617)
4. Cardozo, T., and M. Pagano. 2004. The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5:739-751.
5. Davis, M., et al. 2002. Pseudosubstrate regulation of the SCF(beta-TrCP) ubiquitin ligase by hnRNP-U. Genes Dev. 16:439-451. (Pubitemid 34165101)
6. Grim, J. E., et al. 2008. Isoform- and cell cycle-dependent substrate degradation by the Fbw7 ubiquitin ligase. J. Cell Biol. 181:913-920. (Pubitemid 351846825)
7. Gu, Z., K. Inomata, K. Ishizawa, and A. Horii. 2007. The FBXW7 beta-form is suppressed in human glioma cells. Biochem. Biophys. Res. Commun. 354:992-998.
8. Gupta-Rossi, N., et al. 2001. Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J. Biol. Chem. 276:34371-34378.
9. Gustafson, M. P., M. Welcker, H. C. Hwang, and B. E. Clurman. 2005. Zcchc8 is a glycogen synthase kinase-3 substrate that interacts with RNA-binding proteins. Biochem. Biophys. Res. Commun. 338:1359-1367.
10. Hao, B., S. Oehlmann, M. E. Sowa, J. W. Harper, and N. P. Pavletich. 2007. Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases. Mol. Cell 26:131-143.
11. Hedgepeth, C. M., M. A. Deardorff, K. Rankin, and P. S. Klein. 1999. Regulation of glycogen synthase kinase 3β and downstream Wnt signaling by axin. Mol. Cell. Biol. 19:7147-7157.
12. Huber, M. D., J. H. Dworet, K. Shire, L. Frappier, and M. A. McAlear. 2000. The budding yeast homolog of the human EBNA1-binding protein 2 (Ebp2p) is an essential nucleolar protein required for pre-rRNA processing. J. Biol. Chem. 275:28764-28773.
13. Jager, S., J. Strayle, W. Heinemeyer, and D. H. Wolf. 2001. Cic1, an adaptor protein specifically linking the 26S proteasome to its substrate, the SCF component Cdc4. EMBO J. 20:4423-4431.
14. Kapoor, P., B. D. Lavoie, and L. Frappier. 2005. EBP2 plays a key role in Epstein-Barr virus mitotic segregation and is regulated by aurora family kinases. Mol. Cell. Biol. 25:4934-4945.
15. Kapoor, P., K. Shire, and L. Frappier. 2001. Reconstitution of Epstein-Barr virus-based plasmid partitioning in budding yeast. EMBO J. 20:222-230. (Pubitemid 32099118)
16. Kemp, Z., et al. 2005. CDC4 mutations occur in a subset of colorectal cancers but are not predicted to cause loss of function and are not associated with chromosomal instability. Cancer Res. 65:11361-11366. (Pubitemid 41821693)
17. Kimura, T., M. Gotoh, Y. Nakamura, and H. Arakawa. 2003. hCDC4b, a regulator of cyclin E, as a direct transcriptional target of p53. Cancer Sci. 94:431-436. (Pubitemid 36790475)
18. Koepp, D. M., et al. 2001. Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294:173-177. (Pubitemid 32952972)
19. Malyukova, A., et al. 2007. The tumor suppressor gene hCDC4 is frequently mutated in human T-cell acute lymphoblastic leukemia with functional consequences for Notch signaling. Cancer Res. 67:5611-5616. (Pubitemid 46984990)
20. Maser, R. S., et al. 2007. Chromosomally unstable mouse tumours have genomic alterations similar to diverse human cancers. Nature 447:966-971. (Pubitemid 46975753)
21. Matsumoto, A., I. Onoyama, and K. I. Nakayama. 2006. Expression of mouse Fbxw7 isoforms is regulated in a cell cycle- or p53-dependent manner. Biochem. Biophys. Res. Commun. 350:114-119.
22. Moberg, K. H., D. W. Bell, D. C. Wahrer, D. A. Haber, and I. K. Hariharan. 2001. Archipelago regulates cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 413:311-316.
23. Nakayama, K. I., and K. Nakayama. 2006. Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 6:369-381.
24. Nash, P., et al. 2001. Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414:514-521. (Pubitemid 33131529)
25. Nateri, A. S., L. Riera-Sans, C. Da Costa, and A. Behrens. 2004. The ubiquitin ligase SCFFbw7 antagonizes apoptotic JNK signaling. Science 303:1374-1378. (Pubitemid 38269431)
26. Nayyar, V. K., K. Shire, and L. Frappier. 2009. Mitotic chromosome interactions of Epstein-Barr nuclear antigen 1 (EBNA1) and human EBNA1-binding protein 2 (EBP2). J. Cell Sci. 122:4341-4350.
27. Oberg, C., et al. 2001. The Notch intracellular domain is ubiquitinated and negatively regulated by the mammalian Sel-10 homolog. J. Biol. Chem. 276:35847-35853.
28. O'Neil, J., et al. 2007. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J. Exp. Med. 204:1813-1824.
29. Orlicky, S., X. Tang, A. Willems, M. Tyers, and F. Sicheri. 2003. Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 112:243-256. (Pubitemid 36144113)
30. Patton, E. E., A. R. Willems, and M. Tyers. 1998. Combinatorial control in ubiquitin-dependent proteolysis: don't Skp the F-box hypothesis. Trends Genet. 14:236-243. (Pubitemid 28266975)
31. Petroski, M. D., and R. J. Deshaies. 2005. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6:9-20.
32. Pierce, N. W., G. Kleiger, S. O. Shan, and R. J. Deshaies. 2009. Detection of sequential polyubiquitylation on a millisecond timescale. Nature 462:615-619.
33. Popov, N., C. Schulein, L. A. Jaenicke, and M. Eilers. 2010. Ubiquitylation of the amino terminus of Myc by SCF(beta-TrCP) antagonizes SCF(Fbw7)-mediated turnover. Nat. Cell Biol. 12:973-981.
34. Rajagopalan, H., et al. 2004. Inactivation of hCDC4 can cause chromosomal instability. Nature 428:77-81. (Pubitemid 38332360)
35. Reimers, K., et al. 2001. NoBP, a nuclear fibroblast growth factor 3 binding protein, is cell cycle regulated and promotes cell growth. Mol. Cell. Biol. 21:4996-5007.
36. Romanova, L., et al. 2009. Critical role of nucleostemin in pre-rRNA processing. J. Biol. Chem. 284:4968-4977.
37. Shirai, C., and K. Mizuta. 2008. SUMO mediates interaction of Ebp2p, the yeast homolog of Epstein-Barr virus nuclear antigen 1-binding protein 2, with a RING finger protein Ris1p. Biosci. Biotechnol. Biochem. 72:1881-1886.
38. Shire, K., D. F. Ceccarelli, T. M. Avolio-Hunter, and L. Frappier. 1999. EBP2, a human protein that interacts with sequences of the Epstein-Barr virus nuclear antigen 1 important for plasmid maintenance. J. Virol. 73:2587-2595. (Pubitemid 29135642)
39. Skowyra, D., K. L. Craig, M. Tyers, S. J. Elledge, and J. W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219.
40. Spruck, C. H., et al. 2002. hCDC4 gene mutations in endometrial cancer. Cancer Res. 62:4535-4539.
41. Strohmaier, H., et al. 2001. Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413:316-322. (Pubitemid 32905853)
42. Tang, X., et al. 2007. Suprafacial orientation of the SCF(Cdc4) dimer accommodates multiple geometries for substrate ubiquitination. Cell 129:1165-1176. (Pubitemid 46891040)
43. Thompson, B. J., et al. 2007. The SCFFBW7 ubiquitin ligase complex as a tumor suppressor in T cell leukemia. J. Exp. Med. 204:1825-1835.
44. Tsujii, R., et al. 2000. Ebp2p, yeast homologue of a human protein that interacts with Epstein-Barr virus nuclear antigen 1, is required for pre-rRNA processing and ribosomal subunit assembly. Genes Cells 5:543-553. (Pubitemid 30602697)
45. van Drogen, F., et al. 2006. Ubiquitylation of cyclin E requires the sequential function of SCF complexes containing distinct hCdc4 isoforms. Mol. Cell 23:37-48. (Pubitemid 43963444)
46. Wei, W., J. Jin, S. Schlisio, J. W. Harper, and W. G. Kaelin, Jr. 2005. The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin ligase. Cancer Cell 8:25-33.
47. Welcker, M., and B. E. Clurman. 2008. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 8:83-93.
48. Welcker, M., and B. E. Clurman. 2005. The SV40 large T antigen contains a decoy phosphodegron that mediates its interactions with Fbw7/hCdc4. J. Biol. Chem. 280:7654-7658.
49. Welcker, M., A. Orian, J. E. Grim, R. N. Eisenman, and B. E. Clurman. 2004. A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Curr. Biol. 14:1852-1857.
50. Welcker, M., et al. 2004. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc. Natl. Acad. Sci. U. S. A. 101:9085-9090.
51. Welcker, M., et al. 2003. Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation. Mol. Cell 12:381-392. (Pubitemid 37238925)
52. Wu, G., et al. 2001. SEL-10 is an inhibitor of notch signaling that targets notch for ubiquitin-mediated protein degradation. Mol. Cell. Biol. 21:7403-7415.
53. Wu, H., D. F. Ceccarelli, and L. Frappier. 2000. The DNA segregation mechanism of Epstein-Barr virus nuclear antigen 1. EMBO Rep. 1:140-144.
54. Yada, M., et al. 2004. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 23:2116-2125. (Pubitemid 38737738)
55. Ye, X., et al. 2004. Recognition of phosphodegron motifs in human cyclin E by the SCF(Fbw7) ubiquitin ligase. J. Biol. Chem. 279:50110-50119.