Discovery of a potential allosteric ligand binding site in CDK2

ACS Chemical Biology

Volumn 6, Issue 5, 2011, Pages 492-501

  Betzi, Stephane ^a   Alam, Riazul ^a   Martin, Mathew ^a   Lubbers, Donna J ^a   Han, Huijong ^a   Jakkaraj, Sudhakar R ^b   Georg, Gunda I ^b   Schönbrunn, Ernst ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ADENOSINE TRIPHOSPHATE; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 2 INHIBITOR; CYCLINE; JWS 648; SU 9516; UNCLASSIFIED DRUG;

ALLOSTERISM; BINDING AFFINITY; CONFERENCE PAPER; CRYSTALLOGRAPHY; DRUG BINDING; DRUG BINDING SITE; DRUG SYNTHESIS; ENZYME ASSAY; FLUORESCENCE SPECTROSCOPY; HUMAN; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

ALLOSTERIC SITE; ANILINO NAPHTHALENESULFONATES; CRYSTALLOGRAPHY, X-RAY; CYCLIN A; CYCLIN-DEPENDENT KINASE 2; HUMANS; IMIDAZOLES; INDOLES; LIGANDS; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE;

EID: 79957497448     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb100410m     Document Type: Conference Paper

References (46)

1. Hall, M. and Peters, G. (1996) Genetic alterations of cyclins, cyclin-dependent kinases, and Cdk inhibitors in human cancer Adv. Cancer. Res. 68, 67-108 (Pubitemid 26099813)
2. Johnson, L. N. (2009) Protein kinase inhibitors: contributions from structure to clinical compounds Q. Rev. Biophys. 42, 1-40
3. Zhang, J., Yang, P. L., and Gray, N. S. (2009) Targeting cancer with small molecule kinase inhibitors Nat. Rev. Cancer 9, 28-39
4. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I., Arthur, J. S., Alessi, D. R., and Cohen, P. (2007) The selectivity of protein kinase inhibitors: a further update Biochem. J. 408, 297-315
5. Sherr, C. J. (1996) Cancer cell cycles Science 274, 1672-1677
6. Grana, X. and Reddy, E. P. (1995) Cell cycle control in mammalian cells: role of cyclins, cyclin dependent kinases (CDKs), growth suppressor genes and cyclin-dependent kinase inhibitors (CKIs) Oncogene 11, 211-219
7. Morgan, D. O. (1995) Principles of CDK regulation Nature 374, 131-134
8. Ortega, S., Malumbres, M., and Barbacid, M. (2002) Cyclin D-dependent kinases, INK4 inhibitors and cancer Biochim. Biophys. Acta 1602, 73-87 (Pubitemid 34311901)
9. Weinberg, R. A. (1995) The retinoblastoma protein and cell cycle control Cell 81, 323-330
10. van den Heuvel, S. and Harlow, E. (1993) Distinct roles for cyclin-dependent kinases in cell cycle control Science 262, 2050-2054 (Pubitemid 24041887)
11. Malumbres, M. and Barbacid, M. (2001) To cycle or not to cycle: a critical decision in cancer Nat. Rev. Cancer 1, 222-231 (Pubitemid 33741897)
12. Echalier, A., Endicott, J. A., and Noble, M. E. (2010) Recent developments in cyclin-dependent kinase biochemical and structural studies Biochim. Biophys. Acta 1804, 511-519
13. Liu, Y. and Gray, N. S. (2006) Rational design of inhibitors that bind to inactive kinase conformations Nat. Chem. Biol. 2, 358-364 (Pubitemid 43936934)
14. Russo, A. A., Jeffrey, P. D., Patten, A. K., Massague, J., and Pavletich, N. P. (1996) Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex Nature 382, 325-331 (Pubitemid 26260452)
15. Gondeau, C., Gerbal-Chaloin, S., Bello, P., Aldrian-Herrada, G., Morris, M. C., and Divita, G. (2005) Design of a novel class of peptide inhibitors of cyclin-dependent kinase/cyclin activation J. Biol. Chem. 280, 13793-13800 (Pubitemid 40517276)
16. McInnes, C., Andrews, M. J., Zheleva, D. I., Lane, D. P., and Fischer, P. M. (2003) Peptidomimetic design of CDK inhibitors targeting the recruitment site of the cyclin subunit Curr. Med. Chem. Anticancer Agents 3, 57-69 (Pubitemid 36131635)
17. Kontopidis, G., Andrews, M. J., McInnes, C., Plater, A., Innes, L., Renachowski, S., Cowan, A., and Fischer, P. M. (2009) Truncation and optimization of peptide inhibitors of cyclin-dependent kinase 2-cyclin a through structure-guided design ChemMedChem 4, 1120-1128
18. Mendoza, N., Fong, S., Marsters, J., Koeppen, H., Schwall, R., and Wickramasinghe, D. (2003) Selective cyclin-dependent kinase 2/cyclin A antagonists that differ from ATP site inhibitors block tumor growth Cancer Res. 63, 1020-1024 (Pubitemid 36278433)
19. Cowan-Jacob, S. W., Fendrich, G., Floersheimer, A., Furet, P., Liebetanz, J., Rummel, G., Rheinberger, P., Centeleghe, M., Fabbro, D., and Manley, P. W. (2007) Structural biology contributions to the discovery of drugs to treat chronic myelogenous leukaemia Acta Crystallogr. D: Biol. Crystallogr. 63, 80-93 (Pubitemid 46141483)
20. Ohren, J. F., Chen, H., Pavlovsky, A., Whitehead, C., Zhang, E., Kuffa, P., Yan, C., McConnell, P., Spessard, C., Banotai, C., Mueller, W. T., Delaney, A., Omer, C., Sebolt-Leopold, J., Dudley, D. T., Leung, I. K., Flamme, C., Warmus, J., Kaufman, M., Barrett, S., Tecle, H., and Hasemann, C. A. (2004) Structures of human MAP kinase kinase 1 (MEK1) and MEK2 describe novel noncompetitive kinase inhibition Nat. Struct. Mol. Biol. 11, 1192-1197
21. Pargellis, C., Tong, L., Churchill, L., Cirillo, P. F., Gilmore, T., Graham, A. G., Grob, P. M., Hickey, E. R., Moss, N., Pav, S., and Regan, J. (2002) Inhibition of p38 MAP kinase by utilizing a novel allosteric binding site Nat. Struct. Biol. 9, 268-72 (Pubitemid 34289898)
22. Zuccotto, F., Ardini, E., Casale, E., and Angiolini, M. (2010) Through the "gatekeeper door": exploiting the active kinase conformation J. Med. Chem. 53, 2681-2694
23. Kluter, S., Grutter, C., Naqvi, T., Rabiller, M., Simard, J. R., Pawar, V., Getlik, M., and Rauh, D. (2010) Displacement assay for the detection of stabilizers of inactive kinase conformations J. Med. Chem. 53, 357-367
24. Schonbrunn, E., Eschenburg, S., Luger, K., Kabsch, W., and Amrhein, N. (2000) Structural basis for the interaction of the fluorescence probe 8-anilino-1-naphthalene sulfonate (ANS) with the antibiotic target MurA Proc. Natl. Acad. Sci. U.S.A. 97, 6345-6349 (Pubitemid 30412716)
25. Stryer, L. (1965) The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescence probe of non-polar binding sites J. Mol. Biol. 13, 482-495
26. Heitz, F., Morris, M. C., Fesquet, D., Cavadore, J. C., Doree, M., and Divita, G. (1997) Interactions of cyclins with cyclin-dependent kinases: a common interactive mechanism Biochemistry 36, 4995-5003 (Pubitemid 27180982)
27. Morris, M. C., Gondeau, C., Tainer, J. A., and Divita, G. (2002) Kinetic mechanism of activation of the Cdk2/cyclin A complex. Key role of the C-lobe of the Cdk J. Biol. Chem. 277, 23847-23853 (Pubitemid 34952229)
28. Lawrie, A. M., Noble, M. E., Tunnah, P., Brown, N. R., Johnson, L. N., and Endicott, J. A. (1997) Protein kinase inhibition by staurosporine revealed in details of the molecular interaction with CDK2 Nat. Struct. Biol. 4, 796-801
29. Brown, N. R., Noble, M. E., Lawrie, A. M., Morris, M. C., Tunnah, P., Divita, G., Johnson, L. N., and Endicott, J. A. (1999) Effects of phosphorylation of threonine 160 on cyclin-dependent kinase 2 structure and activity J. Biol. Chem. 274, 8746-8756 (Pubitemid 29164672)
30. Gu, J. and Bourne, P. E. (2007) Identifying allosteric fluctuation transitions between different protein conformational states as applied to Cyclin Dependent Kinase 2 BMC Bioinf. 8, 45
31. Simard, J. R., Getlik, M., Grutter, C., Schneider, R., Wulfert, S., and Rauh, D. (2010) Fluorophore labeling of the glycine-rich loop as a method of identifying inhibitors that bind to active and inactive kinase conformations J. Am. Chem. Soc. 132, 4152-4160
32. Cox, K. J., Shomin, C. D., and Ghosh, I. (2011) Tinkering outside the kinase ATP box: allosteric (type IV) and bivalent (type V) inhibitors of protein kinases Future Med. Chem. 3, 29-43
33. Stevenson-Lindert, L. M., Fowler, P., and Lew, J. (2003) Substrate specificity of CDK2-cyclin A. What is optimal? J. Biol. Chem. 278, 50956-50960 (Pubitemid 38020328)
34. Adams, J. A., McGlone, M. L., Gibson, R., and Taylor, S. S. (1995) Phosphorylation modulates catalytic function and regulation in the cAMP-dependent protein kinase Biochemistry 34, 2447-2454
35. Cook, P. F., Neville, M. E., Jr., Vrana, K. E., Hartl, F. T., and Roskoski, R., Jr. (1982) Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: kinetic mechanism for the bovine skeletal muscle catalytic subunit Biochemistry 21, 5794-5799
36. Weber, G. and Young, L. B. (1964) Fragmentation of bovine serum albumin by pepsin. I. The origin of the acid expansion of the albumin molecule J. Biol. Chem. 239, 1415-1423
37. Puchaslki, M. M., Morra, M. J., and von Wandruszka, R. (1991) Assessment of inner filter effect corrections in fluorimetry, Fresenius J. Anal. Chem. 340, 341 - 344 (and cited herein
38. Lakowicz, L. (1983) Principles of Fluorescence Spectroscopy, Plenum Press, NY).
39. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallogr. 26, 795-800
40. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D: Biol. Crystallogr. 54, 905-921
41. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta. Crystallogr. D: Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
42. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models Acta. Crystallogr. A 47 (Pt 2) 110-119
43. Kleywegt, G. J., Zou, J.-Y., Kjeldgaard, M., and Jones, T. A. (2001) Around O in International Tables for Crystallography (Rossmann, M. G. and Arnold, E., Eds.), pp 353 - 356, International Union of Crystallography, Chester.
44. DeLano, W. L. (2008) PyMOL Molecular Graphics System, DeLano Scientific LLC, Palo Alto, CA, http://www.pymol.org.
45. Jaroslav, S., Jaroslav, N., and Zdenek, B. (1978) 2,4-Diamino-6-phenyl-1, 3,5-triazines Collect. Czech. Chem. Commun. 43, 1639-1646
46. Cheng, K. Y., Noble, M. E., Skamnaki, V., Brown, N. R., Lowe, E. D., Kontogiannis, L., Shen, K., Cole, P. A., Siligardi, G., and Johnson, L. N. (2006) The role of the phospho-CDK2/cyclin A recruitment site in substrate recognition J. Biol. Chem. 281, 23167-23179