How does activation loop phosphorylation modulate catalytic activity in the cAMP-dependent protein kinase: A theoretical study

Protein Science

Volumn 15, Issue 4, 2006, Pages 672-683

  Cheng, Yuhui ^a,b   Zhang, Yingkai ^c   McCammon, J Andrew ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

Collective motion; Molecular dynamics; Phosphorylation of Thr 197; Protein kinase A (PKA); QM MM calculations

Indexed keywords

ACETYLCHOLINESTERASE; ADENOSINE TRIPHOSPHATE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENOLASE;

AB INITIO CALCULATION; ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CATALYSIS; CHEMICAL ANALYSIS; CORRELATION COEFFICIENT; ELECTRICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME STABILITY; HYDROGEN BOND; MODULATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SIMULATION;

CATALYSIS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; KINETICS; MODELS, MOLECULAR; MODELS, THEORETICAL; MUTATION; PHOSPHORYLATION; PROTEIN CONFORMATION; QUANTUM THEORY; STRUCTURE-ACTIVITY RELATIONSHIP; THREONINE;

EID: 33645523760     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.051852306     Document Type: Article

References (58)

1. Adams, J.A. 2003. Activation loop phosphorylation and catalysis in protein kinases: Is there functional evidence for the autoinhibitor model? Biochemistry 42: 601-607.
2. 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.
3. Amadei, A., Linssen, A.B.M., and Berendsen, H.J.C. 1993. Essential dynamics of proteins. Proteins 17: 412-425.
4. Balsera, M.A., Wriggers, W., Oono, Y., and Schulten, K. 1996. Principal component analysis and long time protein dynamics. J. Phys. Chem. 100: 2567-2572.
5. Bartels, C. and Karplus, M. 1998. Probability distributions for complex systems: Adaptive umbrella sampling of the potential energy. J. Phys. Chem. B 102: 865-880.
6. Becker, O.M. 1997. Geometric versus topological clustering: An insight into conformation mapping. Proteins 27: 213-226.
7. Blume-Jensen, P. and Hunter, T. 2001. Oncogenic kinase signalling. Nature 411: 355-365.
8. Bossemeyer, D. 1995. Protein-kinases - Structure and function. FEBS Lett. 369: 57-61.
9. 2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). EMBO J. 12: 849-859.
10. Cheng, Y., Zhang, Y., and McCammon, J.A. 2005. How does the cAMP-dependent protein kinase catalyze the phosphorylation reaction: An ab initio QM/MM study. J. Am. Chem. Soc. 127: 1553-1562.
11. Cisneros, G.A., Liu, H., Zhang, Y., and Yang, W. 2003. Ab initio QM/MM study shows there is no general acid in the reaction catalyzed by 4-oxalocrotonate tautornerase. J. Am. Chem. Soc. 125: 10384-10393.
12. Cisneros, G.A., Wang, M., Silinski, P., Fitzgerald, M.C., and Yang, W. 2004. The protein backbone makes important contributions to 4-oxalocrotonate tautomerase enzyme catalysis: Understanding from theory and experiment. Biochemistry 43: 6885-6892.
13. Cohen, P. 2001. The role of protein phosphorylation in human health and disease. The Sir Hans Krebs Medal Lecture. Eur. J. Biochem. 268: 5001-5010.
14. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W., and Kollman, P.A. 1995. A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J. Am. Chem. Soc. 117: 5179-5197.
15. Darden, T., York, D., and Pedersen, L. 1993. Particle mesh ewald - An n.log(n) method for ewald sums in large systems. J. Chem. Phys. 98: 10089-10092.
16. Diaz, N. and Field, M.J. 2004. Insights into the phosphoryl-transfer mechanism of cAMP-dependent protein kinase from quantum chemical calculations and molecular dynamics simulations. J. Am. Chem. Soc. 126: 529-542.
17. Engh, R.A. and Bossemeyer, D. 2001. The protein kinase activity modulation sites: Mechanisms for cellular regulation - Targets for therapeutic intervention. Adv. Enzyme Regul. 41: 121-149.
18. _. 2002. Structural aspects of protein kinase control - Role of conformational flexibility. Pharmacol. Ther. 93: 99-111.
19. Garcia, A.E. 1992. Large-amplitude nonlinear motions in proteins. Phys. Rev. Lett. 68: 2696-2699.
20. Grant, B.D. and Adams, J.A. 1996. Pre-steady-state kinetic analysis of cAMP-dependent protein kinase using rapid quench flow techniques. Biochemistry 35: 2022-2029.
21. Hanks, S.K., Quinn, A.M., and Hunter, T. 1988. The protein-kinase family - Conserved features and deduced phylogeny of the catalytic domains. Science 241: 42-52.
22. Hayward, S., Kitao, A., Hirata, F., and Go, N. 1993. Effect of solvent on collective motions in globular protein. J. Mol. Biol. 234: 1207-1217.
23. Herberg, F.W., Doyle, M.L., Cox, S., and Taylor, S.S. 1999. Dissection of the nucleotide and metal-phosphate binding sites in cAMP-dependent protein kinase. Biochemistry 38: 6352-6360.
24. Hess, B. 2000. Similarities between principal components of protein dynamics and random diffusion. Phys. Rev. E 62: 8438-8448.
25. Hubbard, S.R. 1997. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16: 5572-5581.
26. Ichiye, T. and Karplus, M. 1991. Collective motions in proteins - A covariance analysis of atomic fluctuations in molecular-dynamics and normal mode simulations. Proteins 11: 205-217.
27. Johnson, L.N., Noble, M.E.M., and Owen, D.J. 1996. Active and inactive protein kinases: Structural basis for regulation. Cell 85: 149-158.
28. Johnson, D.A., Akamine, P., Radzio-Andzelm, E., Madhusudan, and Taylor, S.S. 2001. Dynamics of cAMP-dependent protein kinase. Chem. Rev. 101: 2243-2270.
29. Kumar, S., Bouzida, D., Swendsen, R.H., Kollman, P.A., and Rosenberg, J.M. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method. J. Comput. Chem. 13: 1011-1021.
30. Liu, H., Zhang, Y., and Yang, W. 2000. How is the active site of enolase organized to catalyze two different reaction steps? J. Am. Chem. Soc. 122: 6560-6570.
31. Lowe, E.D., Noble, M.E.M., Skamnaki, V.T., Oikonomakos, N.G., Owen, D.J., and Johnson, L.N. 1997. The crystal structure of a phosphorylase kinase peptide substrate complex: Kinase substrate recognition. EMBO J. 16: 6646-6658.
32. Lu, B., Wong, C.F., and McCammon, J.A. 2005. Release of ADP from the catalytic subunit of protein kinase A: A molecular dynamics simulation study. Protein Sci. 14: 159-168.
33. Madhusudan, Trafny, E.A., Xuong, N.H., Adams, J.A., Ten Eyck, L.F., Taylor, S.S., and Sowadski, J.M. 1994. cAMP-dependent protein kinase crystallographic insights into substrate recognition and phosphotransfer. Protein Sci. 3: 176-187.
34. Madhusudan, Akamine, P., Xuong, N.H., and Taylor, S.S. 2002. Crystal structure of a transition state mimic of the catalytic subunit of cAMP-dependent protein kinase. Nat. Struct. Biol. 9: 273-277.
35. McCammon, J.A. and Harvey, S.C. 1986. Dynamics of proteins and nucleic acids. Cambridge University Press, Cambridge, UK.
36. Meagher, K.L., Redman, L.T., and Carlson, H.A. 2003. Development of polyphosphate parameters for use with the amber force field. J. Comput. Chem. 24: 1016-1025.
37. Nolen, B., Taylor, S., and Ghosh, G. 2004. Regulation of protein kinases: Controlling activity through activation segment conformation. Mol. Cell 15: 661-675.
38. Radkiewicz, J.L. and Brooks, C.L. 2000. Protein dynamics in enzymatic catalysis: Exploration of dihydrofolate reductase. J. Am. Chem. Soc. 122: 225-231.
39. Rod, T.H., Radkiewicz, J.L., and Brooks, C.L. 2003. Correlated motion and the effect of distal mutations in dihydrofolate reductase. Proc. Natl. Acad. Sci. 100: 6980-6985.
40. Ryckaert, J.P., Ciccotti, G., and Berendsen, H.J.C. 1977. Numerical-integration of cartesian equations of motion of a system with constraints - Molecular-dynamics of n-alkanes. J. Comput. Phys. 23: 327-341.
41. Seifert, M.H.J., Breitenlechner, C.B., Bossemeyer, D., Huber, R., Holak, T.A., and Engh, R.A. 2002. Phosphorylation and flexibility of cyclic-AMP-dependent protein kinase (PKA) using p-31 NMR spectroscopy. Biochemistry 41: 5968-5977.
42. Skamnaki, V.T., Owen, D.J., Noble, M.E.M., Lowe, E.D., Lowe, G., Oikonomakos, N.G., and Johnson, L.N. 1999. Catalytic mechanism of phosphorylase kinase probed by mutational studies. Biochemistry 38: 14718-14730.
43. Sridhar, C.G., Hines, W.A., and Samulski, E.T. 1974. Polypeptide liquid-crystals - Magnetic-susceptibility, twist elastic-constant, rotational viscosity coefficient, and poly-γ-benzyl-L-glutamate sidechain conformation. J. Chem. Phys. 61: 947-953.
44. Swaminathan, S., Harte, W.E., and Beveridge, D.L. 1991. Investigation of domain-structure in proteins via molecular-dynamics simulation - Application to HIV-1 protease dimer. J. Am. Chem. Soc. 113: 2717-2721.
45. Tai, K., Shen, T., Borjesson, U., Philippopoulos, M., and McCammon, J.A. 2001. Analysis of a 10-ns molecular dynamics simulation of mouse acetylcholinesterase. Biophys. J. 81: 715-724.
46. Taylor, S.S. and Radzio-Andzelm, E. 1994. Three protein-kinase structures define a common motif. Structure 2: 345-355.
47. Torrie, G.M. and Valleau, J.P. 1974. Monte-Carlo free-energy estimates using non-Boltzmann sampling - Application to subcritical Lennard-Jones fluid. Chem. Phys. Lett. 28: 578-581.
48. Valiev, M., Kawai, R., Adams, J.A., and Weare, J.H. 2003. The role of the putative catalytic base in the phosphoryl transfer reaction in a protein kinase: First-principles calculations. J. Am. Chem. Soc. 125: 9926-9927.
49. Valleau, J.P. and Torrie, G.M. 1977. A guide for Monte Carlo for statistical mechanics. Plenum Press, Inc., New York.
50. Verhoeven, J.W. 1996. Glossary of terms used in photochemistry. Pure Appl. Chem. 68: 2223-2286.
51. Zhang, Y. 2005a. Improved pseudobonds for combined ab initio quantum mechanical/molecular mechanical methods. J. Chem. Phys. 122: http://jcp.aip.org.
52. _. 2005b. Pseudobond ab initio QM/MM approach and its applications to enzyme reactions. Theor. Chem. Acc. (in press).
53. Zhang, Y., Lee, T.S., and Yang, W. 1999. A pseudobond approach to combining quantum mechanical and molecular mechanical methods. J. Chem. Phys. 110: 46-54.
54. Zhang, Y., Liu, H., and Yang, W. 2000. Free energy calculation on enzyme reactions with an efficient iterative procedure to determine minimum energy paths on a combined ab initio QM/MM potential energy surface. J. Chem. Phys. 112: 3483-3492.
55. Zhang, Y., Kua, J., and McCammon, J.A. 2002a. Role of the catalytic triad and oxyanion hole in acetylcholinesterase catalysis: An ab initio QM/MM study. J. Am. Chem. Soc. 124: 10572-10577.
56. Zhang, Y., Liu, H., and Yang, W. 2002b. Ab initio QM/MM and free energy calculations of enzyme reactions. In Computational methods for macromolecules: Challenges and applications (eds. T. Schlick and H.H. Gan), pp. 332-354. Springer-Verlag, New York.
57. Zhang, Y., Kua, J., and McCammon, J.A. 2003. Influence of structural fluctuation on enzyme reaction energy barriers in combined quantum mechanical/molecular mechanical studies. J. Phys. Chem. B 107: 4459-4463.
58. Zhou, J. and Adams, J.A. 1997. Is there a catalytic base in the active site of cAMP-dependent protein kinase? Biochemistry 36: 2977-2984.