Amide H/2H exchange reveals communication between the cAMP and catalytic subunit-binding sites in the RIα subunit of protein kinase A

Journal of Molecular Biology

Volumn 323, Issue 2, 2002, Pages 377-386

  Anand, Ganesh S ^a   Hughes, Carrie A ^a   Jones, John M ^a   Taylor, Susan S ^a   Komives, Elizabeth A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cAMP; H 2H exchange; MALDI TOF; Protein kinase; Signal transduction

Indexed keywords

AMIDE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DEUTERIUM; HOLOENZYME; HYDROGEN; PROTEIN SUBUNIT; REGULATOR PROTEIN; SOLVENT;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CATALYSIS; DIMERIZATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MUTAGENESIS; PKA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE;

AMIDES; AMINO ACID SEQUENCE; BINDING SITES; CATALYTIC DOMAIN; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HYDROGEN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SOLVENTS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 0036025308     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00919-1     Document Type: Article

References (29)

1. Krebs, E. G. (1993). Nobel lecture. Protein phosphorylation and cellular regulation I. Biosci. Rep. 13, 127-142.
2. Sutherland, E. W. & Rall, T. W. (1958). Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles. J. Biol. Chem. 232, 1077-1091.
3. Johnson, D. A., Akamine, P., Radzio-Andzelm, E., Madhusudan & Taylor, S. S. (2001). Dynamics of cAMP-dependent protein kinase. Chem. Rev. 101, 2243-2270.
4. Gibson, R. M., Ji-Buechler, Y. & Taylor, S. S. (1997). Interaction of the regulatory and catalytic subunits of cAMP-dependent protein kinase: Electrostatic sites on the Type Iα regulatory subunit. J. Biol. Chem. 272, 16343-16350.
5. Herberg, F. W., Dostmann, W. R. G., Zorn, M., Davis, S. J. & Taylor, S. S. (1994). Crosstalk between domains in the regulatory subunit of cAMP-dependent protein kinase: Influence of amino-terminus on cAMP-binding and holoenzyme formation. Biochemistry, 33, 7485-7494.
6. Øgreid, D. & Doskeland, S. O. (1981). The kinetics of association of cyclic AMP to the two types of binding sites associated with protein kinase II from bovine myocardium. FEBS Letters, 129, 287-292.
7. 3H] adenosine cyclic 3′,5′-phosphate bound to the regulatory moiety of protein kinase I by the catalytic subunit of the kinase. Biochemistry, 22, 1686-1696.
8. Weber, I. T., Steitz, T. A., Bubis, J. & Taylor, S. S. (1987). Predicted structures of the cAMP binding domains of the Type I and II regulatory subunits of cAMP-dependent protein kinase. Biochemistry, 26, 343-351.
9. Øgreid, D., Ekanger, R., Suya, R. H., Miller, J. P. & Døskeland, S. O. (1989). Comparison of the two classes of binding sites (A and B) of type I and type II cyclic-AMP-dependent protein kinases by using cyclic nucleotide analogs. Eur. J. Biochem. 181, 19-31.
10. Herberg, F. W., Taylor, S. S. & Dostmann, W. R. (1996). Active site mutations define the pathway for the cooperative activation of cAMP-dependent protein kinase. Biochemistry, 35, 2934-2942.
11. Huang, L. J. & Taylor, S. S. (1998). Dissecting cAMP binding domain A in the RIα subunit of cAMP-dependent protein kinase: Distinct subsites for recognition of cAMP and the catalytic subunit. J. Biol. Chem. 273, 26739-26746.
12. Knighton, D. R., Zheng, J., Ten Eyck, L. F., Ashford, V. A., Xuong, N.-h., Taylor, S. S. & Sowadski, J. M. (1991). Crystal structure of the catalytic subunit of cAMP-dependent protein kinase. Science, 253, 407-414.
13. Buechler, J. A. & Taylor, S. S. (1990). Differential labeling of the catalytic subunit of cAMP-dependent protein kinase with a water-soluble carbodiimide: Identification of carboxyl groups protected by MgATP and inhibitor peptides. Biochemistry, 29, 1937-1943.
14. Su, Y., Dostmann, W. R. G., Herberg, F. W., Durick, K., Xuong, N.-h., Ten Eyck, L. F. et al. (1995). Regulatory (RIα) subunit of protein kinase A: structure of deletion mutant with cAMP binding domains. Science, 269, 807-819.
15. Diller, T. C., Madhusudan, Xuong, N.-h. & Taylor, S. S. (2001). Molecular basis for regulatory subunit diversity in cAMP-dependent protein kinase: Crystal structure of the Type IIB regulatory subunit. Structure, 9, 73-82.
16. Saraswat, L. D., Ringheim, G. A., Bubis, J. & Taylor, S. S. (1988). Deletion mutants as probes for localizing regions of subunit interaction in cAMP dependent protein kinase. J. Biol. Chem. 263, 18241-18246.
17. Zhang, Z. & Smith, D. L. (1993). Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation. Protein Sci. 2, 522-531.
18. Hoofnagle, A. N., Resing, K. A., Goldsmith, E. J. & Ahn, N. G. (2001). Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange. Proc. Natl. Acad. Sci. USA, 98, 956-961.
19. Mandell, J. G., Falick, A. M. & Komives, E. A. (1998). Identification of protein:protein interfaces by decreased amide proton solvent acessibility. Proc. Natl. Acad. Sci. USA, 95, 14705-14710.
20. Hughes, C. A., Mandell, J. G., Anand, G. S., Stock, A. M. & Komives, E. A. (2001). Phosphorylation causes subtle changes in solvent accessibility at the interdomain interface of methylesterase CheB. J. Mol. Biol. 307, 967-976.
21. Mandell, J. G., Baerga-Ortiz, A., Akashi, S., Takio, K. & Komives, E. A. (2001). Solvent accessibility of the thrombin-thrombomodulin interface. J. Mol. Biol. 306, 575-589.
22. Mandell, J. G., Falick, A. M. & Komives, E. A. (1998). Measurement of amide hydrogen exchange by MALDI-TOF mass spectrometry. Anal. Chem. 70, 3987-3995.
23. Andersen, M. D., Shaffer, J., Jennings, P. A. & Adams, M. R. (2001). Structural characterization of protein kinase A as a function of nucleotide binding: Hydrogen-deuterium exchange studies using MALDI-TOF MS detection. J. Biol. Chem. 276, 14204-14211.
24. Potter, R. L. & Taylor, S. S. (1980). The structural domains of cAMP-dependent protein kinase I. Characterization of two sites of proteolytic cleavage and homologies to cAMP-dependent protein kinase II. J. Biol. Chem. 255, 9706-9712.
25. Ringheim, G. E., Saraswat, L. D., Bubis, J. & Taylor, S. S. (1988). Deletion of cAMP-binding site B in the regulatory subunit of cAMP-dependent protein kinase alters the photoaffinity labeling of site A. J. Biol. Chem. 263, 18247-18252.
26. Gibson, R. M., Ji-Buechler, Y. & Taylor, S. S. (1997). Identification of electrostatic interaction sites between the regulatory and catalytic subunits of cyclic AMP-dependent protein kinase. Protein Sci. 6, 1825-1834.
27. Herberg, F. W., Bell, S. M. & Taylor, S. S. (1993). Expression of the catalytic subunit of cAMP-dependent protein kinase in E. coli: Multiple isozymes reflect different phosphorylation states. Protein Eng. 6, 771-777.
28. Buechler, Y. J., Herberg, F. W. & Taylor, S. S. (1993). Regulation-defective mutants of type-I cAMP-dependent protein kinase - Consequences of replacing arginine-94 and arginine-95. J. Biol. Chem. 268, 16495-16503.
29. Canaves, J. M. & Taylor, S. S. (2002). Classification and phylogenetic analysis of cAMP-dependent kinase regulatory subunit family. J. Mol. Evol. 54, 7-29.