Diversity of Bisubstrate Binding Modes of Adenosine Analogue-Oligoarginine Conjugates in Protein Kinase A and Implications for Protein Substrate Interactions

Journal of Molecular Biology

Volumn 403, Issue 1, 2010, Pages 66-77

  Pflug, Alexander ^a   Rogozina, Jevgenia ^b   Lavogina, Darja ^b   Enkvist, Erki ^b   Uri, Asko ^b   Engh, Richard Alan ^a   Bossemeyer, Dirk ^c  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY OF TARTU   (Estonia)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Bisubstrate; Inhibitor; Oligoarginine; PKA; Protein kinase

Indexed keywords

ADENOSINE DERIVATIVE; ARGININE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ADENOSINE; ENZYME INHIBITOR;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; FLUOROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; ANALOGS AND DERIVATIVES; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ADENOSINE; ARGININE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME INHIBITORS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN STRUCTURE, TERTIARY;

EID: 77957280864     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.08.028     Document Type: Article

References (35)

1. Torkamani A., Verkhivker G., Schork N.J. Cancer driver mutations in protein kinase genes. Cancer Lett. 2009, 281:117-127.
2. Lapenna S., Giordano A. Cell cycle kinases as therapeutic targets for cancer. Nat. Rev., Drug Discov. 2009, 8:547-566.
3. Cohen P. Targeting protein kinases for the development of anti-inflammatory drugs. Curr. Opin. Cell Biol. 2009, 21:317-324.
4. Castoldi R.E., Pennella G., Saturno G.S., Grossi P., Brughera M., Venturi M. Assessing and managing toxicities induced by kinase inhibitors. Curr. Opin. Drug Discov. Dev. 2007, 10:53-57.
5. Lavogina D., Enkvist E., Uri A. Bisubstrate inhibitors of protein kinases: from principle to practical applications. ChemMedChem 2010, 5:23-34.
6. Parang K., Till J.H., Ablooglu A.J., Kohanski R.A., Hubbard S.R., Cole P.A. Mechanism-based design of a protein kinase inhibitor. Nat. Struct. Mol. Biol. 2001, 8:37-41.
7. Shen K., Hines A.C., Schwarzer D., Pickin K.A., Cole P.A. Protein kinase structure and function analysis with chemical tools. Biochim. Biophys. Acta 2005, 1754:65-78.
8. Ramdas L., Obeyesekere N.U., Sun G., McMurray J.S., Budde R.J. N-myristoylation of a peptide substrate for Src converts it into an apparent slow-binding bisubstrate-type inhibitor. J. Pept. Res. 1999, 53:569-577.
9. Ricouart A., Gesquiere J.C., Tartar A., Sergheraert C. Design of potent protein kinases inhibitors using the bisubstrate approach. J. Med. Chem. 1991, 34:73-78.
10. Lavogina D., Lust M., Viil I., König N., Raidaru G., Rogozina J., et al. Structural analysis of ARC-type inhibitor (ARC-1034) binding to protein kinase A catalytic subunit and rational design of bisubstrate analogue inhibitors of basophilic protein kinases. J. Med. Chem. 2009, 52:308-321.
11. Vaasa A., Viil I., Enkvist E., Viht K., Raidaru G., Lavogina D., Uri A. High-affinity bisubstrate probe for fluorescence anisotropy binding/displacement assays with protein kinases PKA and ROCK. Anal. Biochem. 2009, 385:85-93.
12. Lipinski C.A., Lombardo F., Dominy B.W., Feeney P.J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug. Delivery Rev. 2001, 46:3-26.
13. Enkvist E., Lavogina D., Raidaru G., Vaasa A., Viil I., Lust M., et al. Conjugation of adenosine and hexa-(d-arginine) leads to a nanomolar bisubstrate-analog inhibitor of basophilic protein kinases. J. Med. Chem. 2006, 49:7150-7159.
14. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372:774-797.
15. Thompson E.E., Kornev A.P., Kannan N., Kim C., Ten Eyck L.F., Taylor S.S. Comparative surface geometry of the protein kinase family. Protein Sci. 2009, 18:2016-2026.
16. 2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). EMBO J. 1993, 12:849-859.
17. Shugar D. The NTP phosphate donor in kinase reactions: is ATP a monopolist?. Acta Biochim. Pol. 1996, 43:9-23.
18. Gassel M., Breitenlechner C.B., König N., Huber R., Engh R.A., Bossemeyer D. The protein kinase C inhibitor bisindolyl maleimide 2 binds with reversed orientations to different conformations of protein kinase A. J. Biol. Chem. 2004, 279:23679-23690.
19. Caldwell J.J., Davies T.G., Donald A., McHardy T., Rowlands M.G., Aherne G.W., et al. Identification of 4-(4-aminopiperidin-1-yl)-7H-pyrrolo[2,3-d]pyrimidines as selective inhibitors of protein kinase b through fragment elaboration. J. Med. Chem. 2008, 51:2147-2157.
20. Pearson R.B., Kemp B.E. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 1991, 200:62-81.
21. Fujii K., Zhu G., Liu Y., Hallam J., Chen L., Herrero J., Shaw S. Kinase peptide specificity: improved determination and relevance to protein phosphorylation. Proc. Natl Acad. Sci. USA 2004, 101:13744-13749.
22. Wiley J.C., Wailes L.A., Idzerda R.L., McKnight G.S. Role of regulatory subunits and protein kinase inhibitor (PKI) in determining nuclear localization and activity of the catalytic subunit of protein kinase A. J. Biol. Chem. 1999, 274:6381-6387.
23. Kim C., Xuong N., Taylor S.S. Crystal structure of a complex between the catalytic and regulatory (RIα) subunits of PKA. Science 2005, 307:690-696.
24. Kim C., Cheng C.Y., Saldanha S.A., Taylor S.S. PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation. Cell 2007, 130:1032-1043.
25. Brown S.H.J., Wu J., Kim C., Alberto K., Taylor S.S. Novel isoform-specific interfaces revealed by PKA RIIbeta holoenzyme structures. J. Mol. Biol. 2009, 393:1070-1082.
26. Yang J., Cron P., Good V.M., Thompson V., Hemmings B.A., Barford D. Crystal structure of an activated Akt/protein kinase B ternary complex with GSK3-peptide and AMP-PNP. Nat. Struct. Mol. Biol. 2002, 9:940-944.
27. Gassel M., Breitenlechner C.B., Rüger P., Jucknischke U., Schneider T., Huber R., et al. Mutants of protein kinase A that mimic the ATP-binding site of protein kinase B (AKT). J. Mol. Biol. 2003, 329:1021-1034.
28. Wang H., Li M., Lin W., Wang W., Zhang Z., Rayburn E.R., et al. Extracellular activity of cyclic AMP-dependent protein kinase as a biomarker for human cancer detection: distribution characteristics in a normal population and cancer patients. Cancer Epidemiol. Biomark. Prev. 2007, 16:789-795.
29. Studier F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 2005, 41:207-234.
30. Engh R.A., Girod A., Kinzel V., Huber R., Bossemeyer D. Crystal structures of catalytic subunit of cAMP-dependent protein kinase in complex with isoquinolinesulfonyl protein kinase inhibitors H7, H8, and H89. Structural implications for selectivity. J. Biol. Chem. 1996, 271:26157-26164.
31. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 1993, 26:795-800.
32. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Protein Crystallogr. 1992, 26:27-33.
33. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50:760-763. Collaborative Computational Project, Number 4.
34. Schüttelkopf A.W., van Aalten D.M.F. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60:1355-1363.
35. Viht K., Vaasa A., Raidaru G., Enkvist E., Uri A. Fluorometric TLC assay for evaluation of protein kinase inhibitors. Anal. Biochem. 2005, 340:165-170.