Cyclin-dependent kinases: Bridging their structure and function through computations

Future Medicinal Chemistry

Volumn 3, Issue 12, 2011, Pages 1551-1559

  De Vivo, Marco ^a   Bottegoni, Giovanni ^a   Berteotti, Anna ^a   Recanatini, Maurizio ^b   Gervasio, Francesco Luigi ^c   Cavalli, Andrea ^a,b  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; ASPARTIC ACID; CYCLIN A; CYCLIN B; CYCLIN C; CYCLIN D; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 3; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE 8; CYCLIN DEPENDENT KINASE 9; CYCLIN H; ETHISTERONE; GUANOSINE TRIPHOSPHATASE; MAGNESIUM; PHOSPHATE; PHOSPHORYL LIPID A; PROTEIN P107; PROTEIN P130; PROTEIN P35; RNA; SERINE; THREONINE; UNINDEXED DRUG;

COMPUTER SIMULATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; HUMAN; MOLECULAR DYNAMICS; PHOSPHATE TRANSPORT; PLASTICITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTUM MECHANICS; REVIEW;

CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION; MODELS, THEORETICAL; MOLECULAR DYNAMICS SIMULATION; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; QUANTUM THEORY; THERMODYNAMICS;

EID: 80052499578     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.11.113     Document Type: Review

References (61)

1. Morgan DO. Principles of CDK regulation. Nature 374(6518), 131-134 (1995).
2. Mcinnes C. Progress in the evaluation of CDK inhibitors as anti-tumor agents. Drug Discov. Today 13(19-20), 875-881 (2008).
3. Weishaupt JH, Neusch C, Bahr M. Cyclin-dependent kinase 5 (CDK5) and neuronal cell death. Cell Tissue Res. 312(1), 1-8 (2003). (Pubitemid 36578840)
4. Romano G, Giordano A. Role of the cyclin-dependent kinase 9-related pathway in mammalian gene expression and human diseases. Cell Cycle 7(23), 3664-3668 (2008).
5. Cohen P. Protein kinases - the major drug targets of the twenty-first century? Nat. Rev. Drug Discov. 1(4), 309-315 (2002). (Pubitemid 37361447)
6. Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 9(3), 153-166 (2009).
7. Bartkowiak B, Liu P, Phatnani HP et al. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev. 24(20), 2303-2316 (2010).
8. Malumbres M, Harlow E, Hunt T et al. Cyclin-dependent kinases: a family portrait. Nat. Cell Biol. 11(11), 1275-1276 (2009).
9. Dhavan R, Tsai LH. A decade of CDK5. Nat. Rev. Mol. Cell Biol. 2(10), 749-759 (2001). (Pubitemid 33679837)
10. Lilja L, Yang SN, Webb DL, Juntti-βerggren L, Berggren PO, Bark C. Cyclin-dependent kinase 5 promotes insulin exocytosis. J. Biol. Chem. 276(36), 34199-34205 (2001).
11. Price DH. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol. Cell. Biol. 20(8), 2629-2634 (2000). (Pubitemid 30183481)
12. Kobor MS, Greenblatt J. Regulation of transcription elongation by phosphorylation. Biochim. Biophys. Acta 1577(2), 261-275 (2002). (Pubitemid 35223218)
13. Phelps MA, Lin TS, Johnson AJ et al. Clinical response and pharmacokinetics from a phase 1 study of an active dosing schedule of flavopiridol in relapsed chronic lymphocytic leukemia. Blood 113(12), 2637-2645 (2009).
14. Heath EI, Bible K, Martell RE, Adelman DC, Lorusso PM. A phase 1 study of SNS-032 (formerly BMS-387032), a potent inhibitor of cyclin-dependent kinases 2, 7 and 9 administered as a single oral dose and weekly infusion in patients with metastatic refractory solid tumors. Invest. New Drugs 26(1), 59-65 (2008).
15. Nebreda AR. CDK activation by non-cyclin proteins. Curr. Opin. Cell Biol. 18(2), 192-198 (2006). (Pubitemid 43375888)
16. Lolli G, Johnson LN. CAK-cyclin-dependent activating kinase: a key kinase in cell cycle control and a target for drugs? Cell Cycle 4(4), 572-577 (2005). (Pubitemid 41359784)
17. Russo AA, Jeffrey PD, Pavletich NP. Structural basis of cyclin-dependent kinase activation by phosphorylation. Nat. Struct. Biol. 3(8), 696-700 (1996). (Pubitemid 26260060)
18. Endicott JA, Noble MEM, Tucker JA. Cyclin-dependent kinases: inhibition and substrate recognition. Curr. Opin. Struct. Biol. 9(6), 738-744 (1999).
19. Jeffrey PD, Ruso AA, Polyak K et al. Mechanism of CDK activation revealed by the structure of a cyclin-CDK2 complex. Nature 376(6538), 313-320 (1995).
20. Noble MEM, Endicott JA, Johnson LN. Protein kinase inhibitors: insights into drug design from structure. Science 303(5665), 1800-1805 (2004). (Pubitemid 38374863)
21. Knowles JR. Enzyme-catalyzed phosphoryl transfer-reactions. Annu. Rev. Biochem. 49, 877-919 (1980).
22. Holmes RR. Phosphoryl transfer enzymes and hypervalent phosphorus chemistry. Acc. Chem. Res. 37(10), 746-753 (2004).
23. Kamerlin SC, Warshel A. On the energetics of ATP hydrolysis in solution. J. Phys. Chem. B 113(47), 15692-15698 (2009).
24. Baxter NJ, Bowler MW, Alizadeh T et al. Atomic details of near-transition state conformers for enzyme phosphoryl transfer revealed by MgF3- rather than by phosphoranes. Proc. Natl Acad. Sci. USA 107(10), 4555-4560
25. Lahiri SD, Zhang GF, Dunaway-Mariano D, Allen KN. The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science 299(5615), 2067-2071 (2003). (Pubitemid 36383733)
26. Klahn M, Rosta E, Warshel A. On the mechanism of hydrolysis of phosphate monoesters dianions in solutions and proteins. J. Am. Chem. Soc. 128(47), 15310-15323 (2006). (Pubitemid 44853542)
27. De Vivo M, Dal Peraro M, Klein ML. Phosphodiester cleavage in ribonuclease H occurs via an associative two-metal-aided catalytic mechanism. J. Am. Chem. Soc. 130(33), 10955-10962 (2008).
28. Schramm VL. Enzymatic transition states and transition state analogues. Curr. Opin. Struct. Biol. 15(6), 604-613 (2005). (Pubitemid 41668515)
29. Hart JC, Sheppard DW, Hillier IH, Burton NA. What is the mechanism of phosphoryl transfer in protein kinases? A hybrid quantum mechanical/molecular mechanical study. Chem. Comm. (1), 79-80 (1999). (Pubitemid 29037561)
30. Hutter MC, Helms V. Influence of key residues on the reaction mechanism of the cAMP-dependent protein kinase. Protein Sci. 8(12), 2728-2733 (1999). (Pubitemid 30007635)
31. Hirano Y, Hata M, Hoshino T, Tsuda M. Quantum chemical study on the catalytic mechanism of the C-subunit of cAMP-dependent protein kinase. J. Phys. Chem. B 106(22), 5788-5792 (2002). (Pubitemid 35281889)
32. Cavalli A, De Vivo M, Recanatini M. Density functional study of the enzymatic reaction catalyzed by a cyclin-dependent kinase. Chem. Comm. (11), 1308-1309 (2003). (Pubitemid 36649003)
33. De Vivo M, Cavalli A, Carloni P, Recanatini M. Computational study of the phosphoryl transfer catalyzed by a cyclin-dependent kinase. Chemistry 13(30), 8437-8444 (2007). (Pubitemid 47608879)
34. Schlichting I, Reinstein J. Structures of active conformations of UMP kinase from Dictyostelium discoideum suggest phosphoryl transfer is associative. Biochemistry 36(31), 9290-9296 (1997). (Pubitemid 27346965)
35. Schlichting I, Reinstein J. pH influences fluoride coordination number of the AlFx phosphoryl transfer transition state analog. Nat. Struct. Biol. 6(8), 721-723 (1999). (Pubitemid 29360229)
36. Hagopian JC, Kirtley MP, Stevenson LM et al. Kinetic basis for activation of CDK2/clyclin A by phosphorylation. J. Biol. Chem. 276(1), 275-280 (2001). (Pubitemid 32050317)
37. De Vivo M, Ensing B, Dal Peraro M, Gomez GA, Christianson DW, Klein ML. Proton shuttles and phosphatase activity in soluble epoxide hydrolase. J. Am. Chem. Soc. 129(2), 387-394 (2007). (Pubitemid 46106639)
38. De Vivo M, Ensing B, Klein ML. Computational study of phosphatase activity in soluble epoxide hydrolase: high efficiency through a water bridge mediated proton shuttle. J. Am. Chem. Soc. 127(32), 11226-11227 (2005). (Pubitemid 41176867)
39. Diaz N, Field MJ. Insights into the phosphoryl-transfer mechanism of cAMP-dependent protein kinase from quantum chemical calculations and molecular dynamics simulations. J. Am. Chem. Soc. 126(2), 529-542 (2004). (Pubitemid 38088001)
40. Cheng YH, Zhang YK, Mccammon JA. How does the cAMP-dependent protein kinase catalyze the phosphorylation reaction: an ab initio QM/MM study. J. Am. Chem. Soc. 127(5), 1553-1562 (2005).
41. Valiev M, Kawai R, Adams JA, Weare JH. The role of the putative catalytic base in the phosphoryl transfer reaction in a protein kinase: first-principles calculations. J. Am. Chem. Soc. 125(33), 9926-9927 (2003). (Pubitemid 36994914)
42. Seeliger MA, Ranjitkar P, Kasap C et al. Equally potent inhibition of c-Src and Abl by compounds that recognize inactive kinase conformations. Cancer Res. 69(6), 2384-2392 (2009).
43. Shan Y, Seeliger MA, Eastwood MP et al. A conserved protonation-dependent switch controls drug binding in the Abl kinase. Proc. Natl Acad. Sci. USA 106(1), 139-144 (2009).
44. Zhang B, Su ZC, Tay TE, Tan VB. Mechanism of CDK5 activation revealed by steered molecular dynamics simulations and energy calculations. J. Mol. Model. 16(6), 1159-1168 (2010).
45. Kufareva I, Abagyan R. Type-II kinase inhibitor docking, screening, and profiling using modified structures of active kinase states. J. Med. Chem. 51(24), 7921-7932 (2008).
46. Zuccotto F, Ardini E, Casale E, Angiolini M. Through the "gatekeeper door": exploiting the active kinase conformation. J. Med. Chem. 53(7), 2681-2694
47. Garuti L, Roberti M, Bottegoni G. Non-ATP competitive protein kinase inhibitors. Curr. Med. Chem. 17(25), 2804-2821 (2010).
48. Kontopidis G, Mcinnes C, Pandalaneni SR et al. Differential binding of inhibitors to active and inactive CDK2 provides insights for drug design. Chem. Biol. 13(2), 201-211 (2006). (Pubitemid 43255592)
49. Berteotti A, Cavalli A, Branduardi D, Gervasio FL, Recanatini M, Parrinello M. Protein conformational transitions: the closure mechanism of a kinase explored by atomistic simulations. J. Am. Chem. Soc. 131(1), 244-250 (2009).
50. De Vivo M, Cavalli A, Bottegoni G, Carloni P, Recanatini M. Role of phosphorylated Thr160 for the activation of the CDK2/ Cyclin a complex. Proteins 62(1), 89-98 (2006). (Pubitemid 43063007)
51. Brown NR, Noble MEM, Lawrie AM et al. Effects of phosphorylation of threonine 160 on cyclin-dependent kinase 2 structure and activity. J. Biol. Chem. 274(13), 8746-8756 (1999). (Pubitemid 29164672)
52. Mapelli M, Massimiliano L, Crovace C et al. Mechanism of CDK5/p25 binding by CDK inhibitors. J. Med. Chem. 48(3), 671-679 (2005). (Pubitemid 40209090)
53. Tarricone C, Dhavan R, Peng J, Areces LB, Tsai LH, Musacchio A. Structure and regulation of the CDK5-p25(nck5a) complex. Mol. Cell 8(3), 657-669 (2001). (Pubitemid 32946942)
54. Poon RY, Lew J, Hunter T. Identification of functional domains in the neuronal CDK5 activator protein. J. Biol. Chem. 272(9), 5703-5708 (1997). (Pubitemid 27102398)
55. Qi Z, Huang QQ, Lee KY, Lew J, Wang JH. Reconstitution of neuronal Cdc2-like kinase from bacteri-expressed CDK5 and an active fragment of the brain-specific activator. Kinase activation in the absence of CDK5 phosphorylation. J. Biol. Chem. 270(18), 10847-10854 (1995).
56. Laio A, Gervasio FL. Metadynamics: a method to simulate rare events and reconstruct the free energy in biophysics, chemistry and material science. Rep. Prog. Phys. 71, 126601 (2008).
57. Branduardi D, Gervasio FL, Parrinello M. From A to B in free energy space. J. Chem. Phys. 126(5), (2007).
58. Krebs WG, Gerstein M. The morph server: a standardized system for analyzing and visualizing macromolecular motions in a database framework. Nucleic Acids Res. 28(8), 1665-1675 (2000). (Pubitemid 30199298)
59. Xu W, Harrison SC, Eck MJ. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385(6617), 595-602 (1997). (Pubitemid 27087566)
60. Sicheri F, Moarefi I, Kuriyan J. Crystal structure of the Src family tyrosine kinase Hck. Nature 385(6617), 602-609 (1997). (Pubitemid 27087567)
61. Gan W, Yang S, Roux B. Atomistic view of the conformational activation of Src kinase using the string method with swarms-of-trajectories. Biophys. J. 97(4), L8-L10 (2009).