Distinct Activation Pathways Confer Cyclin-Binding Specificity on Cdk1 and Cdk2 in Human Cells

Molecular Cell

Volumn 32, Issue 5, 2008, Pages 662-672

  Merrick, Karl A ^a,b   Larochelle, Stéphane ^a   Zhang, Chao ^c,d   Allen, Jasmina J ^c,d   Shokat, Kevan M ^c,d   Fisher, Robert P ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CELLCYCLE

Indexed keywords

CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2;

ARTICLE; CATALYSIS; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; COMPLEX FORMATION; ENZYME ACTIVATION; ENZYME BINDING; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NONHUMAN; PROTEIN ASSEMBLY;

ANIMALS; CDC2 PROTEIN KINASE; CELL CYCLE; CELL EXTRACTS; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASES; CYCLINS; ENZYME ACTIVATION; ENZYME STABILITY; HCT116 CELLS; HUMANS; MODELS, BIOLOGICAL; PHOSPHATES; PHOSPHORYLATION; PHOSPHOTHREONINE; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY;

METAZOA;

EID: 56849109923     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.10.022     Document Type: Article

References (41)

1. Aleem E., Kiyokawa H., and Kaldis P. Cdc2-cyclin E complexes regulate the G1/S phase transition. Nat. Cell Biol. 7 (2005) 831-836
2. Arooz T., Yam C.H., Siu W.Y., Lau A., Li K.K., and Poon R.Y. On the concentrations of cyclins and cyclin-dependent kinases in extracts of cultured human cells. Biochemistry 39 (2000) 9494-9501
3. Berthet C., Aleem E., Coppola V., Tessarollo L., and Kaldis P. Cdk2 knockout mice are viable. Curr. Biol. 13 (2003) 1775-1785
4. Berthet C., Klarmann K.D., Hilton M.B., Suh H.C., Keller J.R., Kiyokawa H., and Kaldis P. Combined loss of Cdk2 and Cdk4 results in embryonic lethality and Rb hypophosphorylation. Dev. Cell 10 (2006) 563-573
5. Bloom J., and Cross F.R. Multiple levels of cyclin specificity in cell-cycle control. Nat. Rev. Mol. Cell Biol. 8 (2007) 149-160
6. Burkard M.E., Randall C.L., Larochelle S., Zhang C., Shokat K.M., Fisher R.P., and Jallepalli P.V. Chemical genetics reveals the requirement for Polo-like kinase 1 activity in positioning RhoA and triggering cytokinesis in human cells. Proc. Natl. Acad. Sci. USA 104 (2007) 4383-4388
7. Cheng A., Ross K.E., Kaldis P., and Solomon M.J. Dephosphorylation of cyclin-dependent kinases by type 2C protein phosphatases. Genes Dev. 13 (1999) 2946-2957
8. Chow J.P., Siu W.Y., Ho H.T., Ma K.H., Ho C.C., and Poon R.Y. Differential contribution of inhibitory phosphorylation of CDC2 and CDK2 for unperturbed cell cycle control and DNA integrity checkpoints. J. Biol. Chem. 278 (2003) 40815-40828
9. Connell-Crowley L., Solomon M.J., Wei N., and Harper J.W. Phosphorylation-independent activation of human cyclin-dependent kinase 2 by cyclin A in vitro. Mol. Biol. Cell 4 (1993) 79-92
10. De Bondt H.L., Rosenblatt J., Jancarik J., Jones H.D., Morgan D.O., and Kim S.-H. Crystal structure of cyclin-dependent kinase 2. Nature 363 (1993) 595-602
11. Desai D., Gu Y., and Morgan D.O. Activation of human cyclin-dependent kinases in vitro. Mol. Biol. Cell 3 (1992) 571-582
12. Desai D., Wessling H.C., Fisher R.P., and Morgan D.O. The effect of phosphorylation by CAK on cyclin binding by CDC2 and CDK2. Mol. Cell. Biol. 15 (1995) 345-350
13. Fisher R.P. Secrets of a double agent: CDK7 in cell-cycle control and transcription. J. Cell Sci. 118 (2005) 5171-5180
14. Fisher R.P., and Morgan D.O. A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell 78 (1994) 713-724
15. Garrett S., Barton W.A., Knights R., Jin P., Morgan D.O., and Fisher R.P. Reciprocal activation by cyclin-dependent kinases 2 and 7 is directed by substrate specificity determinants outside the T-loop. Mol. Cell. Biol. 21 (2001) 88-99
16. Jeffrey P.D., Russo A.A., Polyak K., Gibbs E., Hurwitz J., Massagué J., and Pavletich N.P. Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376 (1995) 313-320
17. Kaldis P., Russo A.A., Chou H.S., Pavletich N.P., and Solomon M.J. Human and yeast cdk-activating kinases (CAKs) display distinct substrate specificities. Mol. Biol. Cell 9 (1998) 2545-2560
18. Keaton M.A., Bardes E.S., Marquitz A.R., Freel C.D., Zyla T.R., Rudolph J., and Lew D.J. Differential susceptibility of yeast S and M phase CDK complexes to inhibitory tyrosine phosphorylation. Curr. Biol. 17 (2007) 1181-1189
19. L'Italien L., Tanudji M., Russell L., and Schebye X.M. Unmasking the redundancy between Cdk1 and Cdk2 at G2 phase in human cancer cell lines. Cell Cycle 5 (2006) 984-993
20. LaBaer J., Garrett M.D., Stevenson L.F., Slingerland J.M., Sandhu C., Chou H.S., Fattaey A., and Harlow E. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11 (1997) 847-862
21. Larochelle S., Batliner J., Gamble M.J., Barboza N.M., Kraybill B.C., Blethrow J.D., Shokat K.M., and Fisher R.P. Dichotomous but stringent substrate selection by the dual-function Cdk7 complex revealed by chemical genetics. Nat. Struct. Mol. Biol. 13 (2006) 55-62
22. Larochelle S., Chen J., Knights R., Pandur J., Morcillo P., Erdjument-Bromage H., Tempst P., Suter B., and Fisher R.P. T-loop phosphorylation stabilizes the CDK7-cyclin H-MAT1 complex in vivo and regulates its CTD kinase activity. EMBO J. 20 (2001) 3749-3759
23. Larochelle S., Merrick K.A., Terret M.E., Wohlbold L., Barboza N.M., Zhang C., Shokat K.M., Jallepalli P.V., and Fisher R.P. Requirements for Cdk7 in the assembly of Cdk1/cyclin B and activation of Cdk2 revealed by chemical genetics in human cells. Mol. Cell 25 (2007) 839-850
24. Lee K.M., Saiz J.E., Barton W.A., and Fisher R.P. Cdc2 activation in fission yeast depends on Mcs6 and Csk1, two partially redundant Cdk-activating kinases CAKs). Curr. Biol. 9 (1999) 441-444
25. Lolli G., and Johnson L.N. Recognition of Cdk2 by Cdk7. Proteins 67 (2007) 1048-1059
26. Loog M., and Morgan D.O. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 434 (2005) 104-108
27. Malumbres M., Sotillo R., Santamaria D., Galan J., Cerezo A., Ortega S., Dubus P., and Barbacid M. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 118 (2004) 493-504
28. Morgan D.O. The Cell Cycle: Principles of Control (2007), New Science Press Ltd, London
29. Murray A.W., and Marks D. Can sequencing shed light on cell cycling?. Nature 409 (2001) 844-846
30. Ortega S., Prieto I., Odajima J., Martin A., Dubus P., Sotillo R., Barbero J.L., Malumbres M., and Barbacid M. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat. Genet. 35 (2003) 25-31
31. Pagano M., Pepperkok R., Verde F., Ansorge W., and Draetta G. Cyclin A is required at two points in the human cell cycle. EMBO J. 11 (1992) 961-971
32. 160 by the cyclin-dependent kinase-interacting phosphatase KAP in the absence of cyclin. Science 270 (1995) 90-93
33. Rane S.G., Dubus P., Mettus R.V., Galbreath E.J., Boden G., Reddy E.P., and Barbacid M. Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Nat. Genet. 22 (1999) 44-52
34. Ross K.E., Kaldis P., and Solomon M.J. Activating phosphorylation of the Saccharomyces cerevisiae cyclin-dependent kinase, Cdc28p, precedes cyclin binding. Mol. Biol. Cell 11 (2000) 1597-1609
35. Russo A.A., Jeffrey P.D., and Pavletich N.P. Structural basis of cyclin-dependent kinase activation by phosphorylation. Nat. Struct. Biol. 3 (1996) 696-700
36. Saiz J.E., and Fisher R.P. A CDK-activating kinase network is required in cell cycle control and transcription in fission yeast. Curr. Biol. 12 (2002) 1100-1105
37. Santamaria D., Barriere C., Cerqueira A., Hunt S., Tardy C., Newton K., Caceres J.F., Dubus P., Malumbres M., and Barbacid M. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 448 (2007) 811-815
38. Shah K., Liu Y., Deirmengian C., and Shokat K.M. Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc. Natl. Acad. Sci. USA 94 (1997) 3565-3570
39. 2/M in the budding yeast cell cycle. Genetics 147 (1997) 57-71
40. Tsakraklides V., and Solomon M.J. Comparison of Cak1p-like cyclin-dependent kinase-activating kinases. J. Biol. Chem. 277 (2002) 33482-33489
41. Wohlbold L., Larochelle S., Liao J.C., Livshits G., Singer J., Shokat K.M., and Fisher R.P. The cyclin-dependent kinase (CDK) family member PNQALRE/CCRK supports cell proliferation but has no intrinsic CDK-activating kinase (CAK) activity. Cell Cycle 5 (2006) 546-554