Metal-free cAMP-dependent protein kinase can catalyze phosphoryl transfer

Biochemistry

Volumn 53, Issue 19, 2014, Pages 3179-3186

  Gerlits, Oksana ^a   Das, Amit ^a   Keshwani, Malik M ^b   Taylor, Susan ^b   Waltman, Mary Jo ^c   Langan, Paul ^a   Heller, William T ^a   Kovalevsky, Andrey ^a  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COORDINATION REACTIONS; ENZYME ACTIVITY; ENZYME KINETICS; HYDROGEN BONDS; METAL IONS; PEPTIDES;

CATALYTIC SUBUNITS; KINETICS MEASUREMENTS; METAL-BINDING SITES; PHOSPHORYL TRANSFER; PHOSPHORYL TRANSFER REACTIONS; PHOSPHORYLATED PEPTIDES; PHOSPHOTRANSFERASES; SUBSTRATE PEPTIDES;

METALS;

ANIMALS; CATALYTIC DOMAIN; CYCLIC AMP-DEPENDENT PROTEIN KINASE CATALYTIC SUBUNITS; METALS, ALKALI; MICE; PEPTIDES; PHOSPHORYLATION; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS;

EID: 84901049654     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5000965     Document Type: Article

References (49)

1. Adams, J. A. (2001) Kinetic and catalytic mechanisms of protein kinases Chem. Rev. 101, 2271-2290
2. 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
3. Shabb, J. B. (2001) Physiological substrates of cAMP-dependent protein kinase Chem. Rev. 101, 2381-2411
4. Taylor, S. S., Buechler, J. A., and Knighton, D. R. (1990) in Peptides and protein phosphorylation (Kemp, B. E., Ed.), pp 1-41, CRC, Boca Raton, FL.
5. Masterson, L. R., Cheng, C., Yu, T., Tonelli, M., Kornev, A., Taylor, S. S., and Veglia, G. (2010) Dynamics connect substrate recognition to catalysis in protein kinase A Nat. Chem. Biol. 6, 821-828
6. Masterson, L. R., Shi, L., Metcalfe, E., Gao, J., Taylor, S. S., and Veglia, G. (2011) Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 108, 6969-6974
7. Sims, P. C., Moody, I. S., Choi, Y., Dong, C., Iftikhar, M., Corso, B. L., Gul, O. T., Collins, P. G., and Weiss, G. A. (2013) Electronic measurements of single-molecule catalysis by cAMP-dependent protein kinase A J. Am. Chem. Soc. 135, 7861-7868
8. Grant, B. and Adams, J. A. (1996) Pre-steady-state kinetic analysis of cAMP-dependent protein kinase using rapid quench flow techniques Biochemistry 35, 2022-2029
9. Lew, J., Taylor, S. S., and Adams, J. A. (1997) Identification of a partially rate-determining step in the catalytic mechanism of cAMP-dependent protein kinase: A transient kinetic study using stopped-flow fluorescence spectroscopy Biochemistry 36, 6717-6724
10. Shaffer, J. and Adams, J. A. (1999) An ATP-linked structural change in protein kinase A precedes phosphoryl transfer under physiological magnesium concentrations Biochemistry 38, 5572-5581
11. Cox, S., Radzio-Andzelm, E., and Taylor, S. S. (1994) Domain movements in protein kinases Curr. Opin. Struct. Biol. 4, 893-901
12. Shaffer, J. and Adams, J. A. (1999) Detection of conformational changes along the kinetic pathway of protein kinase A using a catalytic trapping technique Biochemistry 38, 12072-12079
13. Armstrong, R. N., Kondo, H., Granot, J., Kaiser, E. T., and Mildvan, A. S. (1979) Magnetic resonance and kinetic studies of the manganese(II) ion and substrate complexes of the catalytic subunit of adenosine 3′,5′- monophosphate dependent protein kinase from bovine heart Biochemistry 18, 1230-1238
14. Armstrong, R. N., Kondo, H., and Kaiser, E. T. (1979) Cyclic AMP-dependent ATPase activity of bovine heart protein kinase Proc. Natl. Acad. Sci. U.S.A. 76, 722-725
15. Bhatnagar, D., Roskoski, R., Jr., Rosendahl, M. S., and Leonard, N. J. (1983) Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: A new fluorescence displacement titration technique for characterizing the nucleotide binding site on the catalytic subunit Biochemistry 22, 6310-6317
16. Zheng, J., Trafny, E. A., Knighton, D. R., Xuong, N. H., Taylor, S. S., Ten Eyck, L. F., and Sowadski, J. M. (1993) 2.2 Å refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor Acta Crystallogr. D49, 362-365
17. Zheng, J., Knighton, D. R., Ten Eyck, L. F., Karlsson, R., Xuong, N.-h., Taylor, S. S., and Sowadski, J. M. (1993) Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MgATP and peptide inhibitor Biochemistry 32, 2154-2161
18. 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
19. Cook, P. F., Neville, M. E., Jr., Vrana, K. E., Hartl, F. T., and Roskoski, R., Jr. (1982) Adenosine cyclic 3′5′-monophosphate dependent protein kinase: Kinetic mechanism for the bovine skeletal muscle catalytic subunit Biochemistry 21, 5794-5799
20. Kovalevsky, A. Y., Johson, H., Hanson, B. L., Waltman, M. J., Fisher, S. Z., Taylor, S., and Langan, P. (2012) Low- and room-temperature X-ray structures of protein kinase A ternary complexes shed new light on its activity Acta Crystallogr. D68, 854-860
21. Valiev, M., Yang, J., Adams, J. A., Taylor, S. S., and Weare, J. H. (2007) Phosphorylation reaction in cAPK protein kinase-Free energy quantum mechanical/molecular mechanics simulations J. Phys. Chem. B 111, 13455-13464
22. 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
23. Szarek, P., Dyguda-Kazimierowicz, E., Tachibana, A., and Sokalski, W. A. (2008) Physical nature of intermolecular interactions within cAMP-dependent protein kinase active site: Differential transition state stabilization in phosphoryl transfer reaction J. Phys. Chem. B 112, 11819-11826
24. Adams, J. A. and Taylor, S. S. (1993) Divalent metal ions influence catalysis and active site accessibility in the cAMP-dependent protein kinase Protein Sci. 2, 2177-2186
25. Gerlits, O., Waltman, M. J., Taylor, S., Langan, P., and Kovalevsky, A. (2013) Insights into the phosphoryl transfer catalyzed by cAMP-dependent protein kinase: An X-ray crystallographic study of complexes with various metals and peptide substrate SP20 Biochemistry 52, 3721-3727
26. Mitchell, R. D., Glass, D. B., Wong, C.-W., Angelos, K. L., and Walsh, D. A. (1995) Heat-stable inhibitor protein derived peptide substrate analogs: Phosphorylation by cAMP-dependent and cGMP-dependent protein kinases Biochemistry 34, 528-534
27. Glass, D. B., Cheng, H.-C., Mueller, L. M., Reed, J., and Walsh, D. A. (1989) Primary structural determinants essential for potent inhibition of cAMP-dependent protein kinase by inhibitory peptides corresponding to the active portion of the heat-stable inhibitor protein J. Biol. Chem. 264, 8802-8810
28. Minor, W., Cymborowski, M., Otwinovski, Z., and Chruszcz, M. (2006) HKL3000: The integration of data reduction and structure solution-from diffraction images to an initial model in minutes Acta Crystallogr. D62, 859-866
29. Sheldrick, G. M. (2008) A short history of SHELX Acta Crystallogr. A: Found. Crystallogr. 64, 112-122
30. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D: Biol. Crystallogr. 66, 213-221
31. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
32. 2+- independent neurexin kinase Cell 133, 328-339
33. Gibbs, C. S. and Zoller, M. J. (1991) Identification of electrostatic interactions that determine the phosphorylation site specificity of the cAMP-dependent protein kinase Biochemistry 30, 5329-5334
34. Gibbs, C. S. and Zoller, M. J. (1991) Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions J. Biol. Chem. 266, 8923-8931
35. Aimes, R. T., Hemmer, W., and Taylor, S. S. (2000) Serine-53 at the tip of the glycine-rich loop of cAMP-dependent protein kinase: Role in catalysis, P-site specificity, and interaction with inhibitors Biochemistry 39, 8325-8332
36. 2--dependent interaction of the inhibitor protein of the cAMP-dependent kinase with the catalytic subunit J. Biol. Chem. 258, 3682-3692
37. 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
38. Qamar, R. and Cook, P. F. (1993) pH dependence of the kinetic mechanism of the adenosine 3′,5′-monophosphate dependent protein kinase catalytic subunit in the direction of magnesium adenosine 5′-dophosphate phosphorylation Biochemistry 32, 6802-6806
39. 2- and other ions in solution Biochem. J. 159, 1-5
40. Alberty, R. A., Smith, R. M., and Bock, R. M. (1951) The apparent ionization constants of the adenosinephosphates and related compounds J. Biol. Chem. 425-434
41. Wilson, J. E. and Chin, A. (1991) Chelation of divalent cations by ATP, studied by titration calorimetry Anal. Biochem. 193, 16-19
42. Montenegro, M., Masgrau, L., Gonzalez-Lafont, A., Lluch, J. M., and Garcia-Viloca, M. (2012) Influence of the enzyme phosphorylation state and the substrate on PKA enzyme dynamics Biophys. Chem. 161, 17-28
43. 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
44. Blow, D. (2000) So do we understand how enzymes work? Structure 8, R77-R81
45. Jencks, W. P. (1986) Catalysis in Chemistry and Enzymology, Dover Publ, New York.
46. Admiraal, S. J. and Herschlag, D. (1995) Mapping the transition state for ATP hydrolysis: implications for enzymatic catalysis Chem. Biol. 2, 729-739
47. Montenegro, M., Garcia-Viloca, M., Lluch, J. M., and Gonzalez-Lafont, A. (2011) A QM/MM study of the phosphoryl transfer to the Kemptide substrate catalyzed by protein kinase A. The effect of the phosphorylation state of the protein on the mechanism Phys. Chem. Chem. Phys. 13, 530-539
48. Creanga, C. and El Murr, N. (2011) Development of new disposable NADH biosensors based on NADH oxidase J. Electroanal. Chem. 656, 179-184
49. Salih, S. G., Khan, J. A., and Newton, R. P. (1988) Cytidine 3′,5′-cyclic monophosphate phosphodiesterase: Immunoreactivity and differential sensitivity to endogenous effectors Biochem. Soc. Trans. 16, 774-775