Targeting diverse signaling interaction sites allows the rapid generation of bivalent kinase inhibitors

ACS Chemical Biology

Volumn 7, Issue 3, 2012, Pages 487-495

  Hill, Zachary B ^a   Perera, B Gayani K ^a   Andrews, Simeon S ^a   Maly, Dustin J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 O ALKYLGUANINE DNA ALKYLTRANSFERASE; ADENOSINE TRIPHOSPHATE; DIVALENT CATION; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE PIM 1; PROTEIN TYROSINE KINASE;

ARTICLE; BINDING SITE; ENZYME BINDING; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEREOCHEMISTRY;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; HEK293 CELLS; HUMANS; LIGANDS; MODELS, MOLECULAR; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84858631510     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200387g     Document Type: Article

References (50)

1. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome Science 298, 1912-1934 (Pubitemid 35425239)
2. Blume-Jensen, P. and Hunter, T. (2001) Oncogenic kinase signalling Nature 411, 355-365 (Pubitemid 32467045)
3. Cohen, P. (2002) Protein kinases-the major drug targets of the twenty-first century? Nat. Rev. Drug Discovery 1, 309-315 (Pubitemid 37361447)
4. Parang, K. and Cole, P. A. (2002) Designing bisubstrate analog inhibitors for protein kinases Pharmacol. Ther. 93, 145-157 (Pubitemid 34615556)
5. 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
6. Ricouart, A., Gesquiere, J. C., Tartar, A., and Sergheraert, C. (1991) Design of potent protein kinase inhibitors using the bisubstrate approach J. Med. Chem. 34, 73-78
7. Hines, A. C. and Cole, P. A. (2004) Design, synthesis, and characterization of an ATP-peptide conjugate inhibitor of protein kinase A Bioorg. Med. Chem. Lett. 14, 2951-2954 (Pubitemid 38569770)
8. Hines, A. C., Parang, K., Kohanski, R. A., Hubbard, S. R., and Cole, P. A. (2005) Bisubstrate analog probes for the insulin receptor protein tyrosine kinase: molecular yardsticks for analyzing catalytic mechanism and inhibitor design Bioorg. Chem. 33, 285-297 (Pubitemid 40962616)
9. Schneider, T. L., Mathew, R. S., Rice, K. P., Tamaki, K., Wood, J. L., and Schepartz, A. (2005) Increasing the kinase specificity of k252a by protein surface recognition Org. Lett. 7, 1695-1698 (Pubitemid 40685341)
10. Lee, J. H., Kumar, S., and Lawrence, D. S. (2008) Stepwise combinatorial evolution of Akt bisubstrate inhibitors ChemBioChem 9, 507-509
11. Meyer, S. C., Shomin, C. D., Gaj, T., and Ghosh, I. (2007) Tethering small molecules to a phage display library: discovery of a selective bivalent inhibitor of protein kinase A J. Am. Chem. Soc. 129, 13812-13813 (Pubitemid 350106063)
12. Shomin, C. D., Meyer, S. C., and Ghosh, I. (2009) Staurosporine tethered peptide ligands that target cAMP-dependent protein kinase (PKA): optimization and selectivity profiling Bioorg. Med. Chem. 17, 6196-6202
13. Stebbins, J. L., De, S. K., Pavlickova, P., Chen, V., Machleidt, T., Chen, L. H., Kuntzen, C., Kitada, S., Karin, M., and Pellecchia, M. (2011) Design and characterization of a potent and selective dual ATP- and substrate-competitive subnanomolar bidentate c-Jun N-terminal kinase (JNK) inhibitor J. Med. Chem. 54, 6206-6214
14. Hah, J. M., Sharma, V., Li, H., and Lawrence, D. S. (2006) Acquisition of a "Group A"-selective Src kinase inhibitor via a global targeting strategy J. Am. Chem. Soc. 128, 5996-5997
15. Profit, A. A., Lee, T. R., Niu, J., and Lawrence, D. S. (2001) Molecular rulers: an assessment of distance and spatial relationships of Src tyrosine kinase Sh2 and active site regions J. Biol. Chem. 276, 9446-9451
16. Hill, Z. B., Perera, B. G., and Maly, D. J. (2009) A chemical genetic method for generating bivalent inhibitors of protein kinases J. Am. Chem. Soc. 131, 6686-6688
17. Hill, Z. B., Perera, B. G., and Maly, D. J. (2011) Bivalent inhibitors of the tyrosine kinases ABL and SRC: determinants of potency and selectivity Mol. BioSyst. 7, 447-456
18. 6- alkylguanine-DNA alkyltransferase for efficient labeling of fusion proteins with small molecules in vivo Chem. Biol. 10, 313-317 (Pubitemid 36516649)
19. Keppler, A., Gendreizig, S., Gronemeyer, T., Pick, H., Vogel, H., and Johnsson, K. (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo Nat. Biotechnol. 21, 86-89 (Pubitemid 36055833)
20. 6-alkylguanine- DNA alkyltransferase with small molecules in vivo and in vitro Methods 32, 437-444 (Pubitemid 38299335)
21. Keppler, A., Pick, H., Arrivoli, C., Vogel, H., and Johnsson, K. (2004) Labeling of fusion proteins with synthetic fluorophores in live cells Proc. Natl. Acad. Sci. U.S.A. 101, 9955-9959 (Pubitemid 38891177)
22. Pick, H., Jankevics, H., and Vogel, H. (2007) Distribution plasticity of the human estrogen receptor alpha in live cells: distinct imaging of consecutively expressed receptors J. Mol. Biol. 374, 1213-1223 (Pubitemid 350122544)
23. Jansen, L. E., Black, B. E., Foltz, D. R., and Cleveland, D. W. (2007) Propagation of centromeric chromatin requires exit from mitosis J. Cell Biol. 176, 795-805 (Pubitemid 46425540)
24. McMurray, M. A. and Thorner, J. (2008) Septin stability and recycling during dynamic structural transitions in cell division and development Curr. Biol. 18, 1203-1208
25. Bojkowska, K., Santoni de Sio, F., Barde, I., Offner, S., Verp, S., Heinis, C., Johnsson, K., and Trono, D. (2011) Measuring in vivo protein half-life Chem. Biol. 18, 805-815
26. Shah, N., Pang, B., Yeoh, K. G., Thorn, S., Chen, C. S., Lilly, M. B., and Salto-Tellez, M. (2008) Potential roles for the PIM1 kinase in human cancer-a molecular and therapeutic appraisal Eur. J. Cancer 44, 2144-2151
27. Bullock, A. N., Debreczeni, J., Amos, A. L., Knapp, S., and Turk, B. E. (2005) Structure and substrate specificity of the Pim-1 kinase J. Biol. Chem. 280, 41675-41682 (Pubitemid 43000572)
28. Hutti, J. E., Jarrell, E. T., Chang, J. D., Abbott, D. W., Storz, P., Toker, A., Cantley, L. C., and Turk, B. E. (2004) A rapid method for determining protein kinase phosphorylation specificity Nat. Methods 1, 27-29
29. 6-benzylguanine (BG). We have found that ATP-competitive inhibitors conjugated to CLP are much more cell-permeable than those that are linked to BG. The difference in cell permeability between the CLP and BG tags has previously been reported: Srikun, D., Albers, A. E., Nam, C. I., Iavarone, A. T., and Chang, C. J. (2010) Organelle-targetable fluorescent probes for imaging hydrogen peroxide in living cells via SNAP-Tag protein labeling J. Am. Chem. Soc. 132, 4455-4465
30. Chen, L. S., Redkar, S., Bearss, D., Wierda, W. G., and Gandhi, V. (2009) Pim kinase inhibitor, SGI-1776, induces apoptosis in chronic lymphocytic leukemia cells Blood 114, 4150-4157
31. Pogacic, V., Bullock, A. N., Fedorov, O., Filippakopoulos, P., Gasser, C., Biondi, A., Meyer-Monard, S., Knapp, S., and Schwaller, J. (2007) Structural analysis identifies imidazo[1,2- b ]pyridazines as PIM kinase inhibitors with in vitro antileukemic activity Cancer Res. 67, 6916-6924 (Pubitemid 47105539)
32. Tanoue, T., Maeda, R., Adachi, M., and Nishida, E. (2001) Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions EMBO J. 20, 466-479 (Pubitemid 32126982)
33. Chang, C. I., Xu, B. E., Akella, R., Cobb, M. H., and Goldsmith, E. J. (2002) Crystal structures of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3b Mol. Cell 9, 1241-1249 (Pubitemid 34722303)
34. Holland, P. M. and Cooper, J. A. (1999) Protein modification: docking sites for kinases Curr. Biol. 9, R329-331
35. Tanoue, T., Adachi, M., Moriguchi, T., and Nishida, E. (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators Nat. Cell Biol. 2, 110-116
36. Rouse, J., Cohen, P., Trigon, S., Morange, M., Alonso-Llamazares, A., Zamanillo, D., Hunt, T., and Nebreda, A. R. (1994) A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins Cell 78, 1027-1037 (Pubitemid 24292330)
37. Lukas, S. M., Kroe, R. R., Wildeson, J., Peet, G. W., Frego, L., Davidson, W., Ingraham, R. H., Pargellis, C. A., Labadia, M. E., and Werneburg, B. G. (2004) Catalysis and function of the p38 alpha.MK2a signaling complex Biochemistry 43, 9950-9960 (Pubitemid 39030885)
38. ter Haar, E., Prabhakar, P., Liu, X., and Lepre, C. (2007) Crystal structure of the p38 alpha-MAPKAP kinase 2 heterodimer J. Biol. Chem. 282, 9733-9739 (Pubitemid 47104583)
39. White, A., Pargellis, C. A., Studts, J. M., Werneburg, B. G., and Farmer, B. T., 2nd (2007) Molecular basis of MAPK-activated protein kinase 2:p38 assembly Proc. Natl. Acad. Sci. U.S.A. 104, 6353-6358 (Pubitemid 47186098)
40. Mayer, R. J. and Callahan, J. F. (2006) p38 MAP kinase inhibitors: A future therapy for inflammatory diseases Drug Discovery Today: Ther. Strategies 3, 49-54
41. Herberich, B., Cao, G. Q., Chakrabarti, P. P., Falsey, J. R., Pettus, L., Rzasa, R. M., Reed, A. B., Reichelt, A., Sham, K., Thaman, M., Wurz, R. P., Xu, S., Zhang, D., Hsieh, F., Lee, M. R., Syed, R., Li, V., Grosfeld, D., Plant, M. H., Henkle, B., Sherman, L., Middleton, S., Wong, L. M., and Tasker, A. S. (2008) Discovery of highly selective and potent p38 inhibitors based on a phthalazine scaffold J. Med. Chem. 51, 6271-6279
42. Cumming, J. G., McKenzie, C. L., Bowden, S. G., Campbell, D., Masters, D. J., Breed, J., and Jewsbury, P. J. (2004) Novel, potent and selective anilinoquinazoline and anilinopyrimidine inhibitors of p38 MAP kinase Bioorg. Med. Chem. Lett. 14, 5389-5394 (Pubitemid 39359133)
43. Sullivan, J. E., Holdgate, G. A., Campbell, D., Timms, D., Gerhardt, S., Breed, J., Breeze, A. L., Bermingham, A., Pauptit, R. A., Norman, R. A., Embrey, K. J., Read, J., VanScyoc, W. S., and Ward, W. H. (2005) Prevention of MKK6-dependent activation by binding to p38alpha MAP kinase Biochemistry 44, 16475-16490 (Pubitemid 41832031)
44. Bardwell, A. J., Frankson, E., and Bardwell, L. (2009) Selectivity of docking sites in MAPK kinases J. Biol. Chem. 284, 13165-13173
45. Citri, A. and Yarden, Y. (2006) EGF-ERBB signalling: towards the systems level Nat. Rev. Mol. Cell Biol. 7, 505-516 (Pubitemid 44036456)
46. Zhang, X., Gureasko, J., Shen, K., Cole, P. A., and Kuriyan, J. (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor Cell 125, 1137-1149 (Pubitemid 43866200)
47. Zhang, X., Pickin, K. A., Bose, R., Jura, N., Cole, P. A., and Kuriyan, J. (2007) Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface Nature 450, 741-744 (Pubitemid 350207680)
48. Muhsin, M., Graham, J., and Kirkpatrick, P. (2003) Gefitinib Nat. Rev. Drug Discovery 2, 515-516
49. Karaman, M. W., Herrgard, S., Treiber, D. K., Gallant, P., Atteridge, C. E., Campbell, B. T., Chan, K. W., Ciceri, P., Davis, M. I., Edeen, P. T., Faraoni, R., Floyd, M., Hunt, J. P., Lockhart, D. J., Milanov, Z. V., Morrison, M. J., Pallares, G., Patel, H. K., Pritchard, S., Wodicka, L. M., and Zarrinkar, P. P. (2008) A quantitative analysis of kinase inhibitor selectivity Nat. Biotechnol. 26, 127-132
50. 6-alkylguanine-DNA alkyltransferase for specific protein labeling in living cells ChemBioChem 6, 1263-1269 (Pubitemid 40978188)