The structure of cyclin E1/CDK2: Implications for CDK2 activation and CDK2-independent roles

EMBO Journal

Volumn 24, Issue 3, 2005, Pages 452-463

  Honda, Reiko ^a   Lowe, Edward D ^a   Dubinina, Elena ^a   Skamnaki, Vicky ^a   Cook, Atlanta ^a   Brown, Nick R ^a   Johnson, Louise N ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cyclin E; Cyclin dependent kinases; Oncogenes; Protein kinase regulation

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; CYCLIN E1; PHOSPHOTHREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CANCER CELL; CELL CYCLE; CELL DIVISION; CENTROSOME; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; GENE OVEREXPRESSION; HUMAN; INSECT CELL; MALIGNANT TRANSFORMATION; MEGAKARYOCYTE; METAZOON; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; TROPHOBLAST; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; CDC2-CDC28 KINASES; CENTROSOME; CRYSTALLOGRAPHY, X-RAY; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLINS; DNA; ENZYME ACTIVATION; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIPROTEIN COMPLEXES; ONCOGENE PROTEINS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

METAZOA;

EID: 14844307019     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600554     Document Type: Article

References (54)

1. Adams JA, McGlone ML, Gibson R, Taylor SS (1995) Phosphorylation modulates catalytic function and regulation in the cAMP-dependent protein kinase. Biochemistry 34: 2447-2454
2. Arooz T, Yam CH, Siu WY, Lau A, Li KK, Poon RY (2000) On the concentrations of cyclins and cyclin-dependent kinases in extracts of cultured human cells. Biochemistry 39: 9494-9501
3. Blanc E, Roversi P, Vonrhein C, Flensberg C, Lea SM, Bricogne G (2004) Refinement of severely incomplete macromolecular structures with BUSTER_TNT. Acta Crystallogr D 60: 2210-2221
4. Bortner DM, Rosenberg MP (1997) Induction of mammary gland hyperplasia and carcinomas in transgenic mice expressing human cyclin E. Mol Cell Biol 17: 453-459
5. Bourne Y, Watson MH, Hickey MJ, Holmes W, Rocque W, Reed SI, Tainer JA (1996) Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle-regulatory protein CksHs1. Cell 84: 863-874
6. Brown NR, Noble ME, Endicott JA, Garman EF, Wakatsuki S, Mitchell E, Rasmussen B, Hunt T, Johnson LN (1995) The crystal structure of cyclin A. Structure 3: 1235-1247
7. Brown NR, Noble ME, Endicott JA, Johnson LN (1999a) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat Cell Biol 1: 438-443
8. Brown NR, Noble ME, Lawrie AM, Morris MC, Tunnah P, Divita G, Johnson LN, Endicott JA (1999b) Effects of phosphorylation of threonine 160 on cyclin-dependent kinase 2 structure and activity. J Biol Chem 274: 8746-8756
9. CCP4 (1994) The CCP4 (Collaborative Computational Project Number 4) suite: programmes for protein crystallography. Acta Crystallogr D 50: 760-763
10. Clurman BE, Sheaff RJ, Thress K, Groudine M, Roberts JM (1996) Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes Dev 10: 1979-1990
11. Cook FN, Neville ME, Vrana KE, Hartl FT, Roskowski R (1982) Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: kinetic mechanism for the bovine skeletal muscle catalytic subunit. Biochemistry 21: 5794-5799
12. Cook JG, Park CH, Burke TW, Leone G, DeGregori J, Engel A, Nevins JR (2002) Analysis of Cdc6 function in the assembly of mammalian prereplication complexes. Proc Natl Acad Sci USA 99: 1347-1352
13. Coverley D, Laman H, Laskey RA (2002) Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat Cell Biol 4: 523-528
14. De Bondt HL, Rosenblatt J, Jancarik J, Jones HD, Morgan DO, Kim SH (1993) Crystal structure of cyclin-dependent kinase 2. Nature 363: 595-602
15. Donnellan R, Chetty R (1999) Cyclin E in human cancers. FASEB J 13: 773-780
16. Ekholm-Reed S, Mendez J, Tedesco D, Zetterberg A, Stillman B, Reed SI (2004) Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J Cell Biol 165: 789-800
17. Geisen C, Moroy T (2002) The oncogenic activity of cyclin E is not confined to Cdk2 activation alone but relies on several other, distinct functions of the protein. J Biol Chem 277: 39909-39918
18. Geng Y, Yu Q, Sicinska E, Das M, Schneider JE, Bhattacharya S, Rideout WM, Bronson RT, Gardner H, Sicinski P (2003) Cyclin E ablation in the mouse. Cell 114: 431-443
19. Jackman M, Kubota Y, den Elzen N, Hagting A, Pines J (2002) Cyclin A and cyclin E CDK2 complexes shuttle between the nucleus and the cytoplasm. Mol Cell Biol 13: 1030-1045
20. Jeffrey PD, Russo AA, Polyak K, Gibbs E, Hurwitz J, Massague J, Pavletich NP (1995) Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376: 313-320
21. Kelly BL, Wolfe KG, Roberts JM (1998) Identification of a substrate-targeting domain in cyclin E necessary for phosphorylation of the retinoblastoma protein. Proc Natl Acad Sci USA 95: 2535-2540
22. Koff A, Cross F, Fisher A, Schumacher J, Leguellec K, Philippe M, Roberts JM (1991) Human cyclin E, a new cyclin that interacts with two members of the CDC2 gene family. Cell 66: 1217-1228
23. Koff A, Giordano A, Desai D, Yamashita K, Harper JW, Elledge S, Nishimoto T, Morgan DO, Franza BR, Roberts JM (1992) Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257: 1689-1694
24. Lauper N, Beck AR, Cariou S, Richman L, Hofmann K, Reith W, Slingerland JM, Amati B (1998) Cyclin E2: a novel CDK2 partner in the late G1 and S phases of the mammalian cell cycle. Oncogene 17: 2637-2643
25. Leatherburrow RJ (1992) GraFit Version 3.0. Erithakus Software, Staines
26. Lee JO, Russo AA, Pavletich NP (1998) Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7. Nature 391: 859-865
27. Leslie AGW (1999) Integration of macro molecular diffraction data. Acta Crystallogr D 10: 1696-1702
28. Lew DJ, Dulic V, Reed SI (1991) Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell 66: 1197-1206
29. Lowe ED, Tews I, Cheng KY, Brown NR, Gul S, Noble ME, Gamblin SJ, Johnson LN (2002) Specificity determinants of recruitment peptides bound to phospho-CDK2/cyclin A. Biochemistry 41: 15625-15634
30. Malumbres M, Hunt SL, Sotillo R, Martin J, Odajima J, Martin A, Dubus P, Ortega S, Barbacid M (2003) Driving the cell cycle to cancer. Adv Exp Med Biol 532: 1-11
31. Matsumoto Y, Maller JL (2004) A centrosomal localization signal in cyclin E required for CDK2-independent S phase entry. Science 306: 885-888
32. Moore JD, Kornbluth S, Hunt T (2002) Identification of the nuclear localisation signal in Xenopus cyclin E and analysis of its role in replication and mitosis. Mol Biol Cell 13: 4388-4400
33. Moroy T, Geisen C (2004) Cyclin E. Int J Biochem Cell Biol 36: 1424-1439
34. Murshudov GN, Vagen AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53: 240-255
35. Orlicky S, Tang X, Willems A, Tyers M, Sicheri F (2003) Structural basis for phosphodependent substrate selection and orientation by the SCF Cdc4 ubiquitin ligase. Cell 112: 243-256
36. Ortega S, Prieto I, Odajima J, Martin A, Dubus P, Sotillo R, Barbero JL, Malumbres M, Barbacid M (2003) Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat Genet 35: 25-31
37. Parisi T, Beck AR, Rougier N, McNeil T, Lucian L, Werb Z, Amati B (2003) Cyclins E1 and E2 are required for endoreplication in placental trophoblast giant cells. EMBO J 22: 4794-4803
38. Porter DC, Zhang N, Danes C, McGahren MJ, Harwell RM, Faruki S, Keyomarsi K (2001) Tumor-specific proteolytic processing of cyclin E generates hyperactive lower-molecular-weight forms. Mol Cell Biol 21: 6254-6269
39. Porter PL, Malone KE, Heagerty PJ, Alexander GM, Gatti LA, Firpo EJ, Daling JR, Roberts JM (1997) Expression of cell-cycle regulators p27Kip1 and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nat Med 3: 222-225
40. Rajagopalan H, Jallepalli PV, Rago C, Velculescu VE, Kinzler KW, Vogelstein B, Lengauer C (2004) Inactivation of hCDC4 can cause chromosomal instability. Nature 428: 77-81
41. Russo AA, Jeffrey PD, Patten AK, Massague J, Pavletich NP (1996a) Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382: 325-331
42. Russo AA, Jeffrey PD, Pavletich NP (1996b) Structural basis of cyclin-dependent kinase activation by phosphorylation. Nat Struct Biol 3: 696-700
43. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385
44. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512
45. Song H, Hanlon N, Brown NR, Noble ME, Johnson LN, Barford D (2001) Phosphoprotein-protein interactions revealed by the crystal structure of kinase-associated phosphatase in complex with phosphoCDK2. Mol Cell 7: 615-626
46. Spruck CH, Strohmaier H, Sangfelt O, Muller HM, Hubalek M, Muller-Holzner E, Marth C, Widschwendter M, Reed SI (2002) hCDC4 gene mutations in endometrial cancer. Cancer Res 62: 4535-4539
47. Spruck CH, Won KA, Reed SI (1999) Deregulated cyclin E induces chromosome instability. Nature 401: 297-300
48. Strausfeld UP, Howell M, Descombes P, Chevalier S, Rempel RE, Adamczewski J, Maller JL, Hunt T, Blow JJ (1996) Both cyclin A and cyclin E have S-phase promoting (SPF) activity in Xenopus egg extracts. J Cell Sci 109 (Part 6): 1555-1563
49. 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
50. Su TT, O'Farrell PH (1998) Chromosome association of minichromosome maintenance proteins in Drosophila endoreplication cycles. J Cell Biol 140: 451-460
51. Tetsu O, McCormick F (2003) Proliferation of cancer cells despite CDK2 inhibition. Cancer Cell 3: 233-245
52. Welker M, Singer J, Loeb KR, Grim J, Bloecher A, Gurien-West M, Clurman BE, Roberts JM (2003) Multisite phosphorylation by CDK2 and GSK3 controls cyclin E degradation. Mol Cell 12: 381-392
53. Won KA, Reed SI (1996) Activation of cyclin E/CDK2 is coupled to site specific autophosphorylation and ubiquitin dependent degradation of cyclin E. EMBO J 15: 4182-4193
54. Zariwala M, Liu J, Xiong Y (1998) Cyclin E2, a novel human G1 cyclin and activating partner of CDK2 and CDK3, is induced by viral oncoproteins. Oncogene 17: 2787-2798