The ubiquitous nature of cancer: The role of the SCFFbw7 complex in development and transformation

Oncogene

Volumn 29, Issue 35, 2010, Pages 4865-4873

  Crusio, K M ^a   King, B ^a   Reavie, L B ^a   Aifantis, I ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Fbw7; GSK 3 ; p53; ubiquitin proteasome system

Indexed keywords

F BOX PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN C MYB; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

CANCER GROWTH; CARCINOGENESIS; HUMAN; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN MODIFICATION; REVIEW; UBIQUITIN PROTEASOME SYSTEM; UBIQUITINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL TRANSFORMATION; ENZYMOLOGY; METABOLISM; NEOPLASMS; PATHOLOGY;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYB; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITINS;

EID: 77956342583     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.222     Document Type: Review

References (80)

1. Akhoondi S, Sun D, von der Lehr N, Apostolidou S, Klotz K, Maljukova A et al. (2007). FBXW7/hCDC4 is a general tumor suppressor in human cancer. Cancer Res 67: 9006-9012.
2. Anand S, Penrhyn-Lowe S, Venkitaraman AR. (2003). AURORA-A amplification overrides the mitotic spindle assembly checkpoint, inducing resistance to Taxol. Cancer Cell 3: 51-62.
3. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW et al. (1996). SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86: 263-274.
4. Barr AR, Gergely F. (2007). Aurora-A: the maker and breaker of spindle poles. J Cell Sci 120(Part 17): 2987-2996.
5. Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, Pagano M. (2008). The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 134: 256-267.
6. Bechard M, Dalton S. (2009). Subcellular localization of glycogen synthase kinase 3beta controls embryonic stem cell self-renewal. Mol Cell Biol 29: 2092-2104.
7. Bhatia K, Huppi K, Spangler G, Siwarski D, Iyer R, Magrath I. (1993). Point mutations in the c-Myc transactivation domain are common in Burkitts lymphoma and mouse plasmacytomas. Nat Genet 5: 56-61.
8. Cartwright P, McLean C, Sheppard A, Rivett D, Jones K, Dalton S. (2005). LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132: 885-896.
9. Cohen P, Frame S. (2001). The renaissance of GSK3. Nat Rev Mol Cell Biol 2: 769-776.
10. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. (1999). Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 13: 2658-2669.
11. Ferrando AA. (2009). The role of NOTCH1 signaling in T-ALL. Hematology Am Soc Hematol Educ Program, 353-361.
12. Finkin S, Aylon Y, Anzi S, Oren M, Shaulian E. (2008). Fbw7 regulates the activity of endoreduplication mediators and the p53 pathway to prevent drug-induced polyploidy. Oncogene 27: 4411-4421.
13. Fryer CJ, White JB, Jones KA. (2004). Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol Cell 16: 509-520.
14. Ganem NJ, Godinho SA, Pellman D. (2009). A mechanism linking extra centrosomes to chromosomal instability. Nature 460: 278-282.
15. Gupta-Rossi N, Le Bail O, Gonen H, Brou C, Logeat F, Six E 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.
16. Hao B, Oehlmann S, Sowa ME, Harper JW, Pavletich NP. (2007). Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphory-lated substrate recognition by SCF ubiquitin ligases. Mol Cell 26: 131-143.
17. Hartwell LH, Mortimer RK, Culotti J, Culotti M. (1973). Genetic control of the cell division cycle in yeast: V. Genetic analysis of cdc mutants. Genetics 74: 267-286.
18. Hemann MT, Bric A, Teruya-Feldstein J, Herbst A, Nilsson JA, Cordon-Cardo C et al. (2005). Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 436: 807-811.
19. Henriksson M, Bakardjiev A, Klein G, Luscher B. (1993). Phospho-rylation sites mapping in the N-terminal domain of c-myc modulate its transforming potential. Oncogene 8: 3199-3209.
20. Hubbard EJ, Wu G, Kitajewski J, Greenwald I. (1997). sel-10, a negative regulator of lin-12 activity in Caenorhabditis elegans, encodes a member of the CDC4 family of proteins. Genes Dev 11: 3182-3193.
21. Ishikawa Y, Onoyama I, Nakayama KI, Nakayama K. (2008). Notch-dependent cell cycle arrest and apoptosis in mouse embryonic fibroblasts lacking Fbxw7. Oncogene 27: 6164-6174.
22. Kane RC, Bross PF, Farrell AT, Pazdur R. (2003). Velcade: U.S. FDA approval for the treatment of multiple myeloma progressing on prior therapy. Oncologist 8: 508-513.
23. Kane RC, Dagher R, Farrell A, Ko CW, Sridhara R, Justice R et al. (2007). Bortezomib for the treatment of mantle cell lymphoma. Clin Cancer Res 13: 5291-5294.
24. Kanei-Ishii C, Nomura T, Takagi T, Watanabe N, Nakayama KI, Ishii S. (2008). Fbxw7 acts as an E3 ubiquitin ligase that targets c-Myb for nemo-like kinase (NLK)-induced degradation. J Biol Chem 283: 30540-30548.
25. Kitagawa K, Hiramatsu Y, Uchida C, Isobe T, Hattori T, Oda T et al. (2009). Fbw7 promotes ubiquitin-dependent degradation of c-Myb: involvement of GSK3-mediated phosphorylation of Thr-572 in mouse c-Myb. Oncogene 28: 2393-2405.
26. Koepp DM, Schaefer LK, Ye X, Keyomarsi K, Chu C, Harper JW et al. (2001). Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294: 173-177.
27. Li J, Pauley AM, Myers RL, Shuang R, Brashler JR, Yan R et al. (2002). SEL-10 interacts with presenilin 1, facilitates its ubiquitina-tion, and alters A-beta peptide production. J Neurochem 82: 1540-1548.
28. Loeb KR, Kostner H, Firpo E, Norwood T, K DT, Clurman BE et al. (2005). A mouse model for cyclin E-dependent genetic instability and tumorigenesis. Cancer Cell 8: 35-47.
29. Love KR, Catic A, Schlieker C, Ploegh HL. (2007). Mechanisms, biology and inhibitors of deubiquitinating enzymes. Nat Chem Biol 3: 697-705.
30. Lowe SW, Sherr CJ. (2003). Tumor suppression by Ink4a-Arf: progress and puzzles. Curr Opin Genet Dev 13: 77-83.
31. Lutterbach B, Hann SR. (1994). Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis. Mol Cell Biol 14: 5510-5522.
32. Mao JH, Kim IJ, Wu D, Climent J, Kang HC, DelRosario R et al. (2008). FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression. Science 321: 1499-1502.
33. Mao JH, Perez-Losada J, Wu D, Delrosario R, Tsunematsu R, Nakayama KI et al. (2004). Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene. Nature 432: 775-779.
34. Maser RS, Choudhury B, Campbell PJ, Feng B, Wong KK, Protopopov A et al. (2007). Chromosomally unstable mouse tumours have genomic alterations similar to diverse human cancers. Nature 447: 966-971.
35. Masuda K, Ishikawa Y, Onoyama I, Unno M, de Alboran IM, Nakayama KI et al. (2010). Complex regulation of cell-cycle inhibitors by Fbxw7 in mouse embryonic fibroblasts. Oncogene 29: 1798-1809.
36. Matsuoka S, Oike Y, Onoyama I, Iwama A, Arai F, Takubo K et al. (2008). Fbxw7 acts as a critical fail-safe against premature loss of hematopoietic stem cells and development of T-ALL. Genes Dev 22: 986-991.
37. Minella AC, Swanger J, Bryant E, Welcker M, Hwang H, Clurman BE. (2002). p53 and p21 form an inducible barrier that protects cells against cyclin E-cdk2 deregulation. Curr Biol 12: 1817-1827.
38. Moberg KH, Bell DW, Wahrer DC, Haber DA, Hariharan IK. (2001). Archipelago regulates cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 413: 311-316.
39. Mukhopadhyay D, Riezman H. (2007). Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315: 201-205.
40. ONeil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C et al. (2007). FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J Exp Med 204: 1813-1824.
41. Oberg C, Li J, Pauley A, Wolf E, Gurney M, Lendahl U. (2001). The Notch intracellular domain is ubiquitinated and negatively regulated by the mammalian Sel-10 homolog. J Biol Chem 276: 35847-35853.
42. Oh IH, Reddy EP. (1999). The myb gene family in cell growth, differentiation and apoptosis. Oncogene 18: 3017-3033.
43. Onoyama I, Tsunematsu R, Matsumoto A, Kimura T, de Alboran IM, Nakayama K et al. (2007). Conditional inactivation of Fbxw7 impairs cell-cycle exit during T cell differentiation and results in lymphomatogenesis. J Exp Med 204: 2875-2888.
44. Palomero T, Odom DT, ONeil J, Ferrando AA, Margolin A, Neuberg DS et al. (2006). Transcriptional regulatory networks downstream of TAL1/SCL in T-cell acute lymphoblastic leukemia. Blood 108: 986-992.
45. Petroski MD. (2008). The ubiquitin system, disease, and drug discovery. BMC Biochem 9(Suppl 1): S7.
46. Pickart CM, Eddins MJ. (2004). Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta 1695: 55-72.
47. Popov N, Herold S, Llamazares M, Schulein C, Eilers M. (2007a). Fbw7 and Usp28 regulate myc protein stability in response to DNA damage. Cell Cycle 6: 2327-2331.
48. Popov N, Wanzel M, Madiredjo M, Zhang D, Beijersbergen R, Bernards R et al. (2007b). The ubiquitin-specific protease USP28 is required for MYC stability. Nat Cell Biol 9: 765-774.
49. Pui JC, Allman D, Xu L, DeRocco S, Karnell FG, Bakkour S et al. (1999). Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 11: 299-308.
50. Rajagopalan H, Jallepalli PV, Rago C, Velculescu VE, Kinzler KW, Vogelstein B et al. (2004). Inactivation of hCDC4 can cause chromosomal instability. Nature 428: 77-81.
51. Reavie L, Gatta GD, Crusio K, Aranda-Orgilles B, Buckley SM, Thompson B et al. (2010). Regulation of hematopoietic stem cell differentiation by a single ubiquitin ligase-substrate complex. Nat Immunol 11: 207-215.
52. Schwartz AL, Ciechanover A. (2009). Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev Pharmacol Toxicol 49: 73-96.
53. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM et al. (2010). Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463: 103-107.
54. Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. (2000). Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev 14: 2501-2514.
55. Siegert W, Beutler C, Langmach K, Keitel C, Schmidt CA. (1990). Differential expression of the oncoproteins c-myc and c-myb in human lymphoproliferative disorders. Eur J Cancer 26: 733-737.
56. Skaar JR, Pagano M. (2009). Control of cell growth by the SCF and APC/C ubiquitin ligases. Curr Opin Cell Biol 21: 816-824.
57. Slamon DJ, Boone TC, Murdock DC, Keith DE, Press MF, Larson RA et al. (1986). Studies of the human c-myb gene and its product in human acute leukemias. Science 233: 347-351.
58. Smith AP, Henze M, Lee JA, Osborn KG, Keck JM, Tedesco D et al. (2006). Deregulated cyclin E promotes p53 loss of heterozygosity and tumorigenesis in the mouse mammary gland. Oncogene 25: 7245-7259.
59. Song L, Rape M. (2008). Reverse the curse-the role of deubiquitination in cell cycle control. Curr Opin Cell Biol 20: 156-163.
60. Soucy TA, Smith PG, Milhollen MA, Berger AJ, Gavin JM, Adhikari S et al. (2009). An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458: 732-736.
61. Spruck CH, Strohmaier H, Sangfelt O, Muller HM, Hubalek M, Muller-Holzner E et al. (2002). hCDC4 gene mutations in endometrial cancer. Cancer Res 62: 4535-4539.
62. Spruck CH, Won KA, Reed SI. (1999). Deregulated cyclin E induces chromosome instability. Nature 401: 297-300.
63. Strohmaier H, Spruck CH, Kaiser P, Won KA, Sangfelt O, Reed SI. (2001). Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413: 316-322.
64. Sundqvist A, Bengoechea-Alonso MT, Ye X, Lukiyanchuk V, Jin J, Harper JW et al. (2005). Control of lipid metabolism by phosphorylation-dependent degradation of the SREBP family of transcription factors by SCF(Fbw7). Cell Metab 1: 379-391.
65. Tan Y, Sangfelt O, Spruck C. (2008). The Fbxw7/hCdc4 tumor suppressor in human cancer. Cancer Lett 271: 1-12.
66. Tetzlaff MT, Yu W, Li M, Zhang P, Finegold M, Mahon K et al. (2004). Defective cardiovascular development and elevated cyclin E and Notch proteins in mice lacking the Fbw7 F-box protein. Proc Natl Acad Sci USA 101: 3338-3345.
67. Thompson BJ, Buonamici S, Sulis ML, Palomero T, Vilimas T, Basso G et al. (2007). The SCFFBW7 ubiquitin ligase complex as a tumor suppressor in T cell leukemia. J Exp Med 204: 1825-1835.
68. Thompson BJ, Jankovic V, Gao J, Buonamici S, Vest A, Lee JM et al. (2008). Control of hematopoietic stem cell quiescence by the E3 ubiquitin ligase Fbw7. J Exp Med 205: 1395-1408.
69. Tsunematsu R, Nakayama K, Oike Y, Nishiyama M, Ishida N, Hatakeyama S et al. (2004). Mouse Fbw7/Sel-10/Cdc4 is required for notch degradation during vascular development. J Biol Chem 279: 9417-9423.
70. Wei W, Jin J, Schlisio S, Harper JW, Kaelin Jr WG. (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.
71. Weissman AM. (2001). Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2: 169-178.
72. Welcker M, Clurman BE. (2007). Fbw7/hCDC4 dimerization regulates its substrate interactions. Cell Div 2: 7.
73. Welcker M, Clurman BE. (2008). FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8: 83-93.
74. Welcker M, Orian A, Grim JE, Eisenman RN, Clurman BE. (2004a). A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Curr Biol 14: 1852-1857.
75. Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN et al. (2004b). The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc Natl Acad Sci USA 101: 9085-9090.
76. Weng AP, Ferrando AA, Lee W, Morris IV JP, Silverman LB, Sanchez-Irizarry C et al. (2004). Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
77. Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H et al. (2004). Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. Embo J 23: 2116-2125.
78. Yano T, Sander CA, Clark HM, Dolezal MV, Jaffe ES, Raffeld M. (1993). Clustered mutations in the second exon of the MYC gene in sporadic Burkitt0s lymphoma. Oncogene 8: 2741-2748.
79. Zhang D, Zaugg K, Mak TW, Elledge SJ. (2006). A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 126: 529-542.
80. Zhou H, Kuang J, Zhong L, Kuo WL, Gray JW, Sahin A et al. (1998). Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat Genet 20: 189-193.