Allosteric regulation of PKCθ: Understanding multistep phosphorylation and priming by ligands in AGC kinases

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 1, 2012, Pages 269-280

  Seco, Jesus ^a   Ferrer Costa, Carles ^a   Campanera, Josep M ^a   Soliva, Robert ^a   Barril, Xavier ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Allosterism; Conformational flexibility; Kinase regulation; Molecular dynamics; PRIE PCA

Indexed keywords

ADENOSINE TRIPHOSPHATE; BISINDOLYLMALEIMIDE; PROTEIN KINASE C INHIBITOR; PROTEIN KINASE C THETA;

ALLOSTERISM; ARTICLE; BINDING SITE; COMPUTER SIMULATION; CONTROLLED STUDY; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CONSERVED SEQUENCE; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ISOENZYMES; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PEPTIDES; PHOSPHORYLATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; THERMODYNAMICS;

EID: 83555176323     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23205     Document Type: Article

References (63)

1. Bridges AJ. Chemical inhibitors of protein kinases. Chem Rev 2001; 101: 2541-2572.
2. Cohen P. Protein kinases--the major drug targets of the twenty-first century? Nat Rev Drug Discov 2002; 1: 309-315.
3. Noble ME, Endicott JA, Johnson LN. Protein kinase inhibitors: insights into drug design from structure. Science 2004; 303: 1800-1805.
4. Calleja V, Laguerre M, Larijani B. 3-D structure and dynamics of protein kinase B-new mechanism for the allosteric regulation of an AGC kinase. J Chem Biol 2009; 2: 11-25.
5. Jeffrey PD, Russo AA, Polyak K, Gibbs E, Hurwitz J, Massague J, Pavletich NP. Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 1995; 376: 313-320.
6. Kufer TA, Sillje HH, Korner R, Gruss OJ, Meraldi P, Nigg EA. Human TPX2 is required for targeting Aurora-A kinase to the spindle. J Cell Biol 2002; 158: 617-623.
7. Anderson K, Yang J, Koretke K, Nurse K, Calamari A, Kirkpatrick RB, Patrick D, Silva D, Tummino PJ, Copeland RA, Lai Z. Binding of TPX2 to Aurora A alters substrate and inhibitor interactions. Biochemistry 2007; 46: 10287-10295.
8. James C, Ugo V, Le Couedic JP, Staerk J, Delhommeau F, Lacout C, Garcon L, Raslova H, Berger R, Bennaceur-Griscelli A, Villeval JL, Constantinescu SN, Casadevall N, Vainchenker W. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 2005; 434: 1144-1148.
9. Calleja V, Alcor D, Laguerre M, Park J, Vojnovic B, Hemmings BA, Downward J, Parker PJ, Larijani B. Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo. PLoS Biol 2007; 5: e95.
10. Zhou YJ, Hanson EP, Chen YQ, Magnuson K, Chen M, Swann PG, Wange RL, Changelian PS, O'Shea JJ. Distinct tyrosine phosphorylation sites in JAK3 kinase domain positively and negatively regulate its enzymatic activity. Proc Natl Acad Sci U S A 1997; 94: 13850-13855.
11. Skaggs BJ, Gorre ME, Ryvkin A, Burgess MR, Xie Y, Han Y, Komisopoulou E, Brown LM, Loo JA, Landaw EM, Sawyers CL, Graeber TG. Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCR-ABL mutants. Proc Natl Acad Sci U S A 2006; 103: 19466-19471.
12. Pearce LR, Komander D, Alessi DR. The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 2010; 11: 9-22.
13. Gunasekaran K, Ma B, Nussinov R. Is allostery an intrinsic property of all dynamic proteins? Proteins 2004; 57: 433-443.
14. del Sol A, Tsai CJ, Ma B, Nussinov R. The origin of allosteric functional modulation: multiple pre-existing pathways. Structure 2009; 17: 1042-1050.
15. Badireddy S, Yunfeng G, Ritchie M, Akamine P, Wu J, Kim CW, Taylor SS, Qingsong L, Swaminathan K, Anand GS. Cyclic AMP analog blocks kinase activation by stabilizing inactive conformation: conformational selection highlights a new concept in allosteric inhibitor design. Mol Cell Proteomics 2011; 10: M110.004390.
16. Masterson LR, Cheng C, Yu T, Tonelli M, Kornev A, Taylor SS, Veglia G. Dynamics connect substrate recognition to catalysis in protein kinase A. Nat Chem Biol 2010; 6: 821-828.
17. Masterson LR, Mascioni A, Traaseth NJ, Taylor SS, Veglia G. Allosteric cooperativity in protein kinase A. Proc Natl Acad Sci U S A 2008; 105: 506-511.
18. Calleja V, Laguerre M, Parker PJ, Larijani B. Role of a novel PH-kinase domain interface in PKB/Akt regulation: structural mechanism for allosteric inhibition. PLoS Biol 2009; 7: e17.
19. Cheng S, Niv MY. Molecular dynamics simulations and elastic network analysis of protein kinase B (Akt/PKB) inactivation. J Chem Inf Model 2010; 50: 1602-1610.
20. Ng YW, Raghunathan D, Chan PM, Baskaran Y, Smith DJ, Lee CH, Verma C, Manser E. Why an A-loop phospho-mimetic fails to activate PAK1: Understanding an inaccessible kinase state by molecular dynamics simulations. Structure 2010; 18: 879-890.
21. Lu SY, Jiang YJ, Zou JW, Wu TX. Molecular modeling and molecular dynamics simulation studies of the GSK3beta/ATP/Substrate complex: Understanding the unique P+4 primed phosphorylation specificity for GSK3beta substrates. J Chem Inf Model 2011;51:1025-1036.
22. Banavali NK, Roux B. Anatomy of a structural pathway for activation of the catalytic domain of Src kinase Hck. Proteins 2007; 67: 1096-1112.
23. Newton AC. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem Rev 2001; 101: 2353-2364.
24. Newton AC. Protein kinase C: poised to signal. Am J Physiol Endocrinol Metab 2010; 298: E395-E402.
25. Le Good JA, Ziegler WH, Parekh DB, Alessi DR, Cohen P, Parker PJ. Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 1998; 281: 2042-2045.
26. Facchinetti V, Ouyang W, Wei H, Soto N, Lazorchak A, Gould C, Lowry C, Newton AC, Mao Y, Miao RQ, Sessa WC, Qin J, Zhang P, Su B, Jacinto E. The mammalian target of rapamycin complex 2 controls folding and stability of Akt and protein kinase C. EMBO J 2008; 27: 1932-1943.
27. Ikenoue T, Inoki K, Yang Q, Zhou X, Guan KL. Essential function of TORC2 in PKC and Akt turn motif phosphorylation, maturation and signalling. EMBO J 2008; 27: 1919-1931.
28. Liu Y, Graham C, Li A, Fisher RJ, Shaw S. Phosphorylation of the protein kinase C-theta activation loop and hydrophobic motif regulates its kinase activity, but only activation loop phosphorylation is critical to in vivo nuclear-factor-kappaB induction. Biochem J 2002; 361: 255-265.
29. Bornancin F, Parker PJ. Phosphorylation of threonine 638 critically controls the dephosphorylation and inactivation of protein kinase Calpha. Curr Biol 1996; 6: 1114-1123.
30. Bornancin F, Parker PJ. Phosphorylation of protein kinase C-alpha on serine 657 controls the accumulation of active enzyme and contributes to its phosphatase-resistant state. J Biol Chem 1997; 272: 3544-3549.
31. Srivastava J, Goris J, Dilworth SM, Parker PJ. Dephosphorylation of PKCdelta by protein phosphatase 2Ac and its inhibition by nucleotides. FEBS Lett 2002; 516: 265-269.
32. Cameron AJ, Escribano C, Saurin AT, Kostelecky B, Parker PJ. PKC maturation is promoted by nucleotide pocket occupation independently of intrinsic kinase activity. Nat Struct Mol Biol 2009; 16: 624-630.
33. Okuzumi T, Fiedler D, Zhang C, Gray DC, Aizenstein B, Hoffman R, Shokat KM. Inhibitor hijacking of Akt activation. Nat Chem Biol 2009; 5: 484-493.
34. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The protein data bank. Nucleic Acids Res 2000; 28: 235-242.
35. Craft JWJr, Legge GB. An AMBER/DYANA/MOLMOL phosphorylated amino acid library set and incorporation into NMR structure calculations. J Biomol NMR 2005; 33: 15-24.
36. Meagher KL, Redman LT, Carlson HA. Development of polyphosphate parameters for use with the AMBER force field. J Comput Chem 2003; 24: 1016-1025.
37. Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TE. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun 1995; 91: 1-41.
38. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983; 79: 926.
39. Leach AR. Molecular modelling: principles and applications. Dorset: Addison-Wesley Longman Ltd; 2001. p 745.
40. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 2003; 24: 1999-2012.
41. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, Chong L, Lee M, Lee T, Duan Y, Wang W, Donini O, Cieplak P, Srinivasan J, Case DA, Cheatham TE, 3rd. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 2000; 33: 889-897.
42. Sitkoff D, Sharp KA, Honig B. Accurate calculation of hydration free energies using macroscopic solvent models. J Phys Chem 1994; 98: 1978-1988.
43. Lazaridis T, Masunov A, Gandolfo F. Contributions to the binding free energy of ligands to avidin and streptavidin. Proteins 2002; 47: 194-208.
44. Hou T, Wang J, Li Y, Wang W. Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J Chem Inf Model 2011; 51: 69-82.
45. Gohlke H, Kiel C, Case DA. Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes. J Mol Biol 2003; 330: 891-913.
46. Tsui V, Case DA. Theory and applications of the generalized Born solvation model in macromolecular simulations. Biopolymers 2000; 56: 275-291.
47. R Development Core Team ( 2010). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0,
48. Hayward S, de Groot BL. Normal modes and essential dynamics. Methods Mol Biol 2008; 443: 89-106.
49. Huse M, Kuriyan J. The conformational plasticity of protein kinases. Cell 2002; 109: 275-282.
50. Smith KJ, Carter PS, Bridges A, Horrocks P, Lewis C, Pettman G, Clarke A, Brown M, Hughes J, Wilkinson M, Bax B, Reith A. The structure of MSK1 reveals a novel autoinhibitory conformation for a dual kinase protein. Structure 2004; 12: 1067-1077.
51. Gassel M, Breitenlechner CB, Konig N, Huber R, Engh RA, 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.
52. Xu ZB, Chaudhary D, Olland S, Wolfrom S, Czerwinski R, Malakian K, Lin L, Stahl ML, Joseph-McCarthy D, Benander C, Fitz L, Greco R, Somers WS, Mosyak L. Catalytic domain crystal structure of protein kinase C-theta (PKCtheta). J Biol Chem 2004; 279: 50401-50409.
53. Komander D, Kular G, Deak M, Alessi DR, van Aalten DM. Role of T-loop phosphorylation in PDK1 activation, stability, and substrate binding. J Biol Chem 2005; 280: 18797-18802.
54. Yang J, Cron P, Good VM, Thompson V, Hemmings BA, Barford D. Crystal structure of an activated Akt/protein kinase B ternary complex with GSK3-peptide and AMP-PNP. Nat Struct Biol 2002; 9: 940-944.
55. Huang X, Begley M, Morgenstern KA, Gu Y, Rose P, Zhao H, Zhu X. Crystal structure of an inactive Akt2 kinase domain. Structure 2003; 11: 21-30.
56. Ikuta M, Kornienko M, Byrne N, Reid JC, Mizuarai S, Kotani H, Munshi SK. Crystal structures of the N-terminal kinase domain of human RSK1 bound to three different ligands: implications for the design of RSK1 specific inhibitors. Protein Sci 2007; 16: 2626-2635.
57. Hauge C, Antal TL, Hirschberg D, Doehn U, Thorup K, Idrissova L, Hansen K, Jensen ON, Jorgensen TJ, Biondi RM, Frodin M. Mechanism for activation of the growth factor-activated AGC kinases by turn motif phosphorylation. EMBO J 2007; 26: 2251-2261.
58. Hindie V, Stroba A, Zhang H, Lopez-Garcia LA, Idrissova L, Zeuzem S, Hirschberg D, Schaeffer F, Jorgensen TJ, Engel M, Alzari PM, Biondi RM. Structure and allosteric effects of low-molecular-weight activators on the protein kinase PDK1. Nat Chem Biol 2009; 5: 758-764.
59. Nishikawa K, Toker A, Johannes FJ, Songyang Z, Cantley LC. Determination of the specific substrate sequence motifs of protein kinase C isozymes. J Biol Chem 1997; 272: 952-960.
60. Czerwinski R, Aulabaugh A, Greco RM, Olland S, Malakian K, Wolfrom S, Lin L, Kriz R, Stahl M, Huang Y, Liu L, Chaudhary D. Characterization of protein kinase C theta activation loop autophosphorylation and the kinase domain catalytic mechanism. Biochemistry 2005; 44: 9563-9573.
61. Gold MG, Barford D, Komander D. Lining the pockets of kinases and phosphatases. Curr Opin Struct Biol 2006; 16: 693-701.
62. Stein A, Pache RA, Bernado P, Pons M, Aloy P. Dynamic interactions of proteins in complex networks: a more structured view. FEBS J 2009; 276: 5390-5405.
63. Shan Y, Seeliger MA, Eastwood MP, Frank F, Xu H, Jensen MO, Dror RO, Kuriyan J, Shaw DE. A conserved protonation-dependent switch controls drug binding in the Abl kinase. Proc Natl Acad Sci U S A 2009; 106: 139-144.