Dynamics connect substrate recognition to catalysis in protein kinase A

Nature Chemical Biology

Volumn 6, Issue 11, 2010, Pages 821-828

  Masterson, Larry R ^a,b   Cheng, Cecilia ^c   Yu, Tao ^b   Tonelli, Marco ^d   Kornev, Alexandr ^c   Taylor, Susan S ^c   Veglia, Gianluigi ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

^c UNIVERSITY OF SAN DIEGO   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE;

ALLOSTERISM; ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENTROPY; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

EID: 77958160823     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.452     Document Type: Article

References (50)

1. Walsh, D. A. & Van Patten, S. M. Multiple pathway signal transduction by the cAMP-dependent protein kinase. FASEB J. 8, 1227-1236 (1994).
2. Shabb, J. B. Physiological substrates of cAMP-dependent protein kinase. Chem. Rev. 101, 2381-2411 (2001).
3. Taylor, S. S. et al. PKA: A portrait of protein kinase dynamics. Biochim. Biophys. Acta 1697, 259-269 (2004).
4. Kornev, A. P. & Taylor, S. S. Defining the conserved internal architecture of a protein kinase. Biochim. Biophys. Acta 1804, 440-444 (2010).
5. Johnson, D. A., Akamine, P., Radzio-Andzelm, E., Madhusudan, M. & Taylor, S. S. Dynamics of cAMP-dependent protein kinase. Chem. Rev. 101, 2243-2270 (2001).
6. Vajpai, N. et al. Solution conformations and dynamics of ABL kinaseinhibitor complexes determined by NMR substantiate the different binding modes of imatinib/nilotinib and dasatinib. J. Biol. Chem. 283, 18292-18302 (2008).
7. Jarymowycz, V. A. & Stone, M. J. Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences. Chem. Rev. 106, 1624-1671 (2006).
8. Popovych, N., Sun, S., Ebright, R. H. & Kalodimos, C. G. Dynamically driven protein allostery. Nat. Struct. Mol. Biol. 13, 831-838 (2006).
9. Marlow, M. S., Dogan, J., Frederick, K. K., Valentine, K. G. & Wand, A. J. The role of conformational entropy in molecular recognition by calmodulin. Nat. Chem. Biol. 6, 352-358 (2010).
10. Gsponer, J. et al. A coupled equilibrium shift mechanism in calmodulinmediated signal transduction. Structure 16, 736-746 (2008).
11. Yao, X., Rosen, M. K. & Gardner, K. H. Estimation of the available free energy in a LOV2-J alpha photoswitch. Nat. Chem. Biol. 4, 491-497 (2008).
12. Mittag, T., Kay, L. E. & Forman-Kay, J. D. Protein dynamics and conformational disorder in molecular recognition. J. Mol. Recognit. 23, 105-116 (2009).
13. Tzeng, S. R. & Kalodimos, C. G. Dynamic activation of an allosteric regulatory protein. Nature 462, 368-372 (2009).
14. Garcia-Viloca, M., Gao, J., Karplus, M. & Truhlar, D. G. How enzymes work: Analysis by modern rate theory and computer simulations. Science 303, 186-195 (2004).
15. Beach, H., Cole, R., Gill, M. L. & Loria, J. P. Conservation of mus-ms enzyme motions in the apo-and substrate-mimicked state. J. Am. Chem. Soc. 127, 9167-9176 (2005).
16. Henzler-Wildman, K. A. et al. A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450, 913-916 (2007).
17. Traaseth, N. J. et al. Structural and dynamic basis of phospholamban and sarcolipin inhibition of ca (2+)-ATPase. Biochemistry 47, 3-13 (2008).
18. Adams, J. A. Kinetic and catalytic mechanisms of protein kinases. Chem. Rev. 101, 2271-2290 (2001).
19. Boehr, D. D., Nussinov, R. & Wright, P. E. The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796 (2009).
20. Mao, D. Y., Ceccarelli, D. F. & Sicheri, F 'Unraveling the tail' of how SRPK1 phosphorylates ASF/SF2. Mol. Cell 29, 535-537 (2008).
21. Masterson, L. R. et al. Expression and purification of isotopically labeled peptide inhibitors and substrates of cAMP-dependant protein kinase A for NMR analysis. Protein Expr. Purif. 64, 231-236 (2009).
22. Masterson, L. R., Mascioni, A., Traaseth, N. J., Taylor, S. S. & Veglia, G. Allosteric cooperativity in protein kinase A. Proc. Natl. Acad. Sci. USA 105, 506-511 (2008).
23. Kay, L. E., Torchia, D. A. & Bax, A. Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28, 8972-8979 (1989).
24. Fenwick, M. K. & Oswald, R. E. NMR spectroscopy of the ligand-binding core of ionotropic glutamate receptor 2 bound to 5-substituted willardiine partial agonists. J. Mol. Biol. 378, 673-685 (2008).
25. Wang, C., Rance, M. & Palmer, A. G. 3rd Mapping chemical exchange in proteins with MW > 50 kD. J. Am. Chem. Soc. 125, 8968-8969 (2003).
26. Shan, Y. et al. A conserved protonation-dependent switch controls drug binding in the abl kinase. Proc. Natl. Acad. Sci. USA 106, 139-144 (2009).
27. Lew, J., Taylor, S. S. & Adams, J. A. Identification of a partially ratedetermining step in the catalytic mechanism of cAMP-dependent protein kinase: A transient kinetic study using stopped-flow fluorescence spectroscopy. Biochemistry 36, 6717-6724 (1997).
28. Massi, F., Wang, C. & Palmer, A. G. 3rd Solution NMR and computer simulation studies of active site loop motion in triosephosphate isomerase. Biochemistry 45, 10787-10794 (2006).
29. Li, F., Juliano, C., Gorfain, E., Taylor, S. S. & Johnson, D. A. Evidence for an internal entropy contributin to phosphoryl transfer: A study of domain clossure, backbone flexibility, and the catalytic cycle of cAMP-dependent protein kinase. J. Mol. Biol. 315, 459-469 (2002).
30. Kim, C., Cheng, C. Y., Saldanha, S. A. & Taylor, S. S. PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation. Cell 130, 1032-1043 (2007).
31. Yang, J. et al. Allosteric network of cAMP-dependent protein kinase revealed by mutation of Tyr204 in the P+1 loop. J. Mol. Biol. 346, 191-201 (2005).
32. Hyeon, C., Jennings, P. A., Adams, J. A. & Onuchic, J. N. Ligand-induced global transitions in the catalytic domain of protein kinase A. Proc. Natl. Acad. Sci. USA 106, 3023-3028 (2009).
33. Wu, J. et al. Crystal structure of the E230Q mutant of cAMP-dependent protein kinase reveals an unexpected apoenzyme conformation and an extended N-terminal A helix. Protein Sci. 14, 2871-2879 (2005).
34. Kamerlin, S. C. & Warshel, A. At the dawn of the 21st century: Is dynamics the missing link for understanding enzyme catalysis? Proteins 78, 1339-1375 (2010).
35. Schwartz, S. D. & Schramm, V. L. Enzymatic transition states and dynamic motion in barrier crossing. Nat. Chem. Biol. 5, 551-558 (2009).
36. Smock, R. G. & Gierasch, L. M. Sending signals dynamically. Science 324, 198-203 (2009).
37. Kumar, S., Ma, B., Tsai, C. J., Sinha, N. & Nussinov, R. Folding and binding cascades: Dynamic landscapes and population shifts. Protein Sci. 9, 10-19 (2000).
38. Hammes, G. G. Multiple conformational changes in enzyme catalysis. Biochemistry 41, 8221-8228 (2002).
39. Hammes-Schiffer, S. & Benkovic, S. J. Relating protein motion to catalysis. Annu. Rev. Biochem. 75, 519-541 (2006).
40. Swain, J. F. & Gierasch, L. M. The changing landscape of protein allostery. Curr. Opin. Struct. Biol. 16, 102-108 (2006).
41. Das, R. et al. Dynamically driven ligand selectivity in cyclic nucleotide binding domains. J. Biol. Chem. 284, 23682-23696 (2009).
42. Müller, C. W., Schlauderer, G. J., Reinstein, J. & Schulz, G. E. Adenylate kinase motions during catalysis: An energetic counterweight balancing substrate binding. Structure 4, 147-156 (1996).
43. Grünberg, R., Nilges, M. & Leckner, J. Flexibility and conformational entropy in protein-protein binding. Structure 14, 683-693 (2006).
44. Mauldin, R. V., Carroll, M. J. & Lee, A. L. Dynamic dysfunction in dihydrofolate reductase results from antifolate drug binding: Modulation of dynamics within a structural state. Structure 17, 386-394 (2009).
45. Masterson, L. R. et al. Backbone NMR resonance assignment of the catalytic subunit of cAMP-dependent protein kinase A in complex with AMP-PNP. Biomol. NMR Assign. 3, 115-117 (2009).
46. Minor, W., Tomchick, D. & Otwinowski, Z. Strategies for macromolecular synchrotron crystallography. Structure 8, R105-R110 (2000).
47. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. & Bax, A. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
48. Farrow, N. A. et al. Backbone dynamics of a free and phosphopeptidecomplexed src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33, 5984-6003 (1994).
49. Pervushin, K., Riek, R., Wider, G. & Wuthrich, K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 94, 12366-12371 (1997).
50. Tjandra, N., Wingfield, P., Stahl, S. & Bax, A. Anisotropic rotational diffusion of perdeuterated HIV protease from 15N NMR relaxation measurements at two magnetic fields. J. Biomol. NMR 8, 273-284 (1996).