Quantitative Proteomics Reveals the Basis for the Biochemical Specificity of the Cell-Cycle Machinery

Molecular Cell

Volumn 43, Issue 3, 2011, Pages 406-417

  Pagliuca, Felicia Walton ^a,b   Collins, Mark O ^c   Lichawska, Agata ^a,b   Zegerman, Philip ^a,b   Choudhary, Jyoti S ^c   Pines, Jonathon ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A2; CYCLIN B1; CYCLIN DEPENDENT KINASE; CYCLIN E;

ARTICLE; BIOCHEMISTRY; CELL CYCLE; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA REPLICATION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MITOSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS;

AMINO ACID SEQUENCE; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE; CYCLIN A2; CYCLIN B1; CYCLIN E; CYCLIN-DEPENDENT KINASES; DNA REPLICATION; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEOMICS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

MAMMALIA;

EID: 79960922610     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.05.031     Document Type: Article

References (73)

1. Abe S., Nagasaka K., Hirayama Y., Kozuka-Hata H., Oyama M., Aoyagi Y., Obuse C., Hirota T. The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. Genes Dev. 2011, 25:863-874.
2. Archambault V., Chang E.J., Drapkin B.J., Cross F.R., Chait B.T., Rout M.P. Targeted proteomic study of the cyclin-Cdk module. Mol. Cell 2004, 14:699-711.
3. Balestrini A., Cosentino C., Errico A., Garner E., Costanzo V. GEMC1 is a TopBP1-interacting protein required for chromosomal DNA replication. Nat. Cell Biol. 2010, 12:484-491.
4. Bentley A.M., Normand G., Hoyt J., King R.W. Distinct sequence elements of cyclin B1 promote localization to chromatin, centrosomes, and kinetochores during mitosis. Mol. Biol. Cell 2007, 18:4847-4858.
5. Blethrow J.D., Glavy J.S., Morgan D.O., Shokat K.M. Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc. Natl. Acad. Sci. USA 2008, 105:1442-1447.
6. Bloom J., Cross F.R. Multiple levels of cyclin specificity in cell-cycle control. Nat. Rev. Mol. Cell Biol. 2007, 8:149-160.
7. Boucrot E., Kirchhausen T. Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl. Acad. Sci. USA 2007, 104:7939-7944.
8. Boulon S., Ahmad Y., Trinkle-Mulcahy L., Verheggen C., Cobley A., Gregor P., Bertrand E., Whitehorn M., Lamond A.I. Establishment of a protein frequency library and its application in the reliable identification of specific protein interaction partners. Mol. Cell. Proteomics 2010, 9:861-879.
9. Brandeis M., Rosewell I., Carrington M., Crompton T., Jacobs M.A., Kirk J., Gannon J., Hunt T. Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc. Natl. Acad. Sci. USA 1998, 95:4344-4349.
10. Cheng K.Y., Noble M.E., Skamnaki V., Brown N.R., Lowe E.D., Kontogiannis L., Shen K., Cole P.A., Siligardi G., Johnson L.N. The role of the phospho-CDK2/cyclin A recruitment site in substrate recognition. J. Biol. Chem. 2006, 281:23167-23179.
11. Chi Y., Welcker M., Hizli A.A., Posakony J.J., Aebersold R., Clurman B.E. Identification of CDK2 substrates in human cell lysates. Genome Biol. 2008, 9:R149.
12. Clute P., Pines J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1999, 1:82-87.
13. Coudreuse D., Nurse P. Driving the cell cycle with a minimal CDK control network. Nature 2010, 468:1074-1079.
14. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
15. Cukier I.H., Li Y., Lee J.M. Cyclin B1/Cdk1 binds and phosphorylates Filamin A and regulates its ability to cross-link actin. FEBS Lett. 2007, 581:1661-1672.
16. den Elzen N., Pines J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 2001, 153:121-136.
17. Dephoure N., Zhou C., Villén J., Beausoleil S.A., Bakalarski C.E., Elledge S.J., Gygi S.P. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 2008, 105:10762-10767.
18. Draviam V.M., Orrechia S., Lowe M., Pardi R., Pines J. The localization of human cyclins B1 and B2 determines CDK1 substrate specificity and neither enzyme requires MEK to disassemble the Golgi apparatus. J. Cell Biol. 2001, 152:945-958.
19. Epstein C.B., Cross F.R. CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev. 1992, 6:1695-1706.
20. Errico A., Deshmukh K., Tanaka Y., Pozniakovsky A., Hunt T. Identification of substrates for cyclin dependent kinases. Adv. Enzyme Regul. 2010, 50:375-399.
21. Fisher D.L., Nurse P. A single fission yeast mitotic cyclin B p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins. EMBO J. 1996, 15:850-860.
22. Foisner R., Malecz N., Dressel N., Stadler C., Wiche G. M-phase-specific phosphorylation and structural rearrangement of the cytoplasmic cross-linking protein plectin involve p34cdc2 kinase. Mol. Biol. Cell 1996, 7:273-288.
23. Fowler V.M., Adam E.J. Spectrin redistributes to the cytosol and is phosphorylated during mitosis in cultured cells. J. Cell Biol. 1992, 119:1559-1572.
24. Gavet O., Pines J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell 2010, 18:533-543.
25. Geley S., Kramer E., Gieffers C., Gannon J., Peters J.M., Hunt T. Anaphase-promoting complex/cyclosome-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J. Cell Biol. 2001, 153:137-148.
26. Geng Y., Yu Q., Sicinska E., Das M., Schneider J.E., Bhattacharya S., Rideout W.M., Bronson R.T., Gardner H., Sicinski P. Cyclin E ablation in the mouse. Cell 2003, 114:431-443.
27. Geng Y., Lee Y.M., Welcker M., Swanger J., Zagozdzon A., Winer J.D., Roberts J.M., Kaldis P., Clurman B.E., Sicinski P. Kinase-independent function of cyclin E. Mol. Cell 2007, 25:127-139.
28. Hagting A., Karlsson C., Clute P., Jackman M., Pines J. MPF localization is controlled by nuclear export. EMBO J. 1998, 17:4127-4138.
29. Heald R., McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 1990, 61:579-589.
30. Holland A.J., Taylor S.S. Cyclin-B1-mediated inhibition of excess separase is required for timely chromosome disjunction. J. Cell Sci. 2006, 119:3325-3336.
31. Hu F., Aparicio O.M. Swe1 regulation and transcriptional control restrict the activity of mitotic cyclins toward replication proteins in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 2005, 102:8910-8915.
32. Huertas P. DNA resection in eukaryotes: deciding how to fix the break. Nat. Struct. Mol. Biol. 2010, 17:11-16.
33. Jackman M., Kubota Y., den Elzen N., Hagting A., Pines J. Cyclin A- and cyclin E-Cdk complexes shuttle between the nucleus and the cytoplasm. Mol. Biol. Cell 2002, 13:1030-1045.
34. Kalaszczynska I., Geng Y., Iino T., Mizuno S., Choi Y., Kondratiuk I., Silver D.P., Wolgemuth D.J., Akashi K., Sicinski P. Cyclin A is redundant in fibroblasts but essential in hematopoietic and embryonic stem cells. Cell 2009, 138:352-365.
35. Kim S.Y., Ferrell J.E. Substrate competition as a source of ultrasensitivity in the inactivation of Wee1. Cell 2007, 128:1133-1145.
36. Kimura K., Hirano M., Kobayashi R., Hirano T. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science 1998, 282:487-490.
37. King R.W., Peters J.M., Tugendreich S., Rolfe M., Hieter P., Kirschner M.W. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 1995, 81:279-288.
38. Kittler R., Pelletier L., Heninger A.K., Slabicki M., Theis M., Miroslaw L., Poser I., Lawo S., Grabner H., Kozak K., et al. Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat. Cell Biol. 2007, 9:1401-1412.
39. Koepp D.M., Schaefer L.K., Ye X., Keyomarsi K., Chu C., Harper J.W., Elledge S.J. Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 2001, 294:173-177.
40. Koff A., Cross F., Fisher A., Schumacher J., Leguellec K., Philippe M., Roberts J.M. Human cyclin E, a new cyclin that interacts with two members of the CDC2 gene family. Cell 1991, 66:1217-1228.
41. Kozar K., Ciemerych M.A., Rebel V.I., Shigematsu H., Zagozdzon A., Sicinska E., Geng Y., Yu Q., Bhattacharya S., Bronson R.T., et al. Mouse development and cell proliferation in the absence of D-cyclins. Cell 2004, 118:477-491.
42. Kraft C., Herzog F., Gieffers C., Mechtler K., Hagting A., Pines J., Peters J.M. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 2003, 22:6598-6609.
43. Kumagai A., Shevchenko A., Shevchenko A., Dunphy W.G. Treslin collaborates with TopBP1 in triggering the initiation of DNA replication. Cell 2010, 140:349-359.
44. Kunda P., Baum B. The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol. 2009, 19:174-179.
45. Lees E., Faha B., Dulic V., Reed S.I., Harlow E. Cyclin E/cdk2 and cyclin A/cdk2 kinases associate with p107 and E2F in a temporally distinct manner. Genes Dev. 1992, 6:1874-1885.
46. Lew D.J., Dulić V., Reed S.I. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell 1991, 66:1197-1206.
47. Li C., Andrake M., Dunbrack R., Enders G.H. A bifunctional regulatory element in human somatic Wee1 mediates cyclin A/Cdk2 binding and Crm1-dependent nuclear export. Mol. Cell. Biol. 2010, 30:116-130.
48. Litovchick L., Sadasivam S., Florens L., Zhu X., Swanson S.K., Velmurugan S., Chen R., Washburn M.P., Liu X.S., DeCaprio J.A. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 2007, 26:539-551.
49. Loog M., Morgan D.O. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 2005, 434:104-108.
50. Mochida S., Ikeo S., Gannon J., Hunt T. Regulated activity of PP2A-B55 delta is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J. 2009, 28:2777-2785.
51. Moore J.D., Kirk J.A., Hunt T. Unmasking the S-phase-promoting potential of cyclin B1. Science 2003, 300:987-990.
52. Murphy M., Stinnakre M.G., Senamaud-Beaufort C., Winston N.J., Sweeney C., Kubelka M., Carrington M., Bréchot C., Sobczak-Thépot J. Delayed early embryonic lethality following disruption of the murine cyclin A2 gene. Nat. Genet. 1997, 15:83-86.
53. Olsen J.V., Vermeulen M., Santamaria A., Kumar C., Miller M.L., Jensen L.J., Gnad F., Cox J., Jensen T.S., Nigg E.A., et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 2010, 3:ra3.
54. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
55. Peter M., Nakagawa J., Dorée M., Labbé J.C., Nigg E.A. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 1990, 61:591-602.
56. Petersen B.O., Lukas J., Sørensen C.S., Bartek J., Helin K. Phosphorylation of mammalian CDC6 by cyclin A/CDK2 regulates its subcellular localization. EMBO J. 1999, 18:396-410.
57. Sanchez-Pulido L., Diffley J.F., Ponting C.P. Homology explains the functional similarities of Treslin/Ticrr and Sld3. Curr. Biol. 2010, 20:R509-R510.
58. Sansam C.L., Cruz N.M., Danielian P.S., Amsterdam A., Lau M.L., Hopkins N., Lees J.A. A vertebrate gene, ticrr, is an essential checkpoint and replication regulator. Genes Dev. 2010, 24:183-194.
59. Santamaría D., Barrière C., Cerqueira A., Hunt S., Tardy C., Newton K., Cáceres J.F., Dubus P., Malumbres M., Barbacid M. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 2007, 448:811-815.
60. Schulman B.A., Lindstrom D.L., Harlow E. Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A. Proc. Natl. Acad. Sci. USA 1998, 95:10453-10458.
61. Stern B., Nurse P. A quantitative model for the cdc2 control of S phase and mitosis in fission yeast. Trends Genet. 1996, 12:345-350.
62. Stewart M.P., Helenius J., Toyoda Y., Ramanathan S.P., Muller D.J., Hyman A.A. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 2011, 469:226-230.
63. Strohmaier H., Spruck C.H., Kaiser P., Won K.A., Sangfelt O., Reed S.I. Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 2001, 413:316-322.
64. Sudakin V., Ganoth D., Dahan A., Heller H., Hershko J., Luca F.C., Ruderman J.V., Hershko A. The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 1995, 6:185-197.
65. Tanaka S., Umemori T., Hirai K., Muramatsu S., Kamimura Y., Araki H. CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 2007, 445:328-332.
66. Toyoshima F., Moriguchi T., Wada A., Fukuda M., Nishida E. Nuclear export of cyclin B1 and its possible role in the DNA damage-induced G2 checkpoint. EMBO J. 1998, 17:2728-2735.
67. Van Leene J., Hollunder J., Eeckhout D., Persiau G., Van De Slijke E., Stals H., Van Isterdael G., Verkest A., Neirynck S., Buffel Y., et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 2010, 6:397.
68. Ward G.E., Kirschner M.W. Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C. Cell 1990, 61:561-577.
69. Watanabe N., Arai H., Iwasaki J., Shiina M., Ogata K., Hunter T., Osada H. Cyclin-dependent kinase (CDK) phosphorylation destabilizes somatic Wee1 via multiple pathways. Proc. Natl. Acad. Sci. USA 2005, 102:11663-11668.
70. Wu J., Vallenius T., Ovaska K., Westermarck J., Mäkelä T.P., Hautaniemi S. Integrated network analysis platform for protein-protein interactions. Nat. Methods 2009, 6:75-77.
71. Yamaguchi T., Goto H., Yokoyama T., Silljé H., Hanisch A., Uldschmid A., Takai Y., Oguri T., Nigg E.A., Inagaki M. Phosphorylation by Cdk1 induces Plk1-mediated vimentin phosphorylation during mitosis. J. Cell Biol. 2005, 171:431-436.
72. Yang J., Bardes E.S., Moore J.D., Brennan J., Powers M.A., Kornbluth S. Control of cyclin B1 localization through regulated binding of the nuclear export factor CRM1. Genes Dev. 1998, 12:2131-2143.
73. Zegerman P., Diffley J.F. Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 2007, 445:281-285.