Phosphodiesterases catalyze hydrolysis of cAMP-bound to regulatory subunit of protein kinase A and mediate signal termination

Molecular and Cellular Proteomics

Volumn 10, Issue 2, 2011, Pages

  Moorthy, Balakrishnan Shenbaga ^a   Gao, Yunfeng ^a   Anand, Ganesh S ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; PHOSPHODIESTERASE; PROTEIN; REGA PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; REGA PROTEIN, BACTERIA;

ALLOSTERISM; ARTICLE; BINDING SITE; CATALYSIS; CELLULAR PARAMETERS; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; DISSOCIATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME REGULATION; FEEDBACK SYSTEM; GENE DELETION; HYDROLYSIS; MASS SPECTROMETRY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TERMINATION; AMINO ACID SEQUENCE; ANIMAL; CATTLE; CHEMISTRY; CONFORMATION; KINETICS; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MOUSE; SPECTROFLUOROMETRY;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CATTLE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; KINETICS; MASS SPECTROMETRY; MICE; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS; SPECTROMETRY, FLUORESCENCE;

EID: 79953225915     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.002295     Document Type: Article

References (52)

1. Berman, H. M., Ten Eyck, L. F., Goodsell, D. S., Haste, N. M., Kornev, A., and Taylor, S. S. (2005) The cAMP binding domain: an ancient signaling module. Proc. Natl. Acad. Sci. U.S.A. 102, 45-50
2. Beebe, S. J., and Corbin, J. D. (1986) Cyclic nucleotide-dependent protein kinases. The Enzymes 17, 43-111
3. Johnson, D. A., Akamine, P., Radzio-Andzelm, E., Madhusudan, M., and Taylor, S. S. (2001) Dynamics of cAMP-dependent protein kinase. Chem. Rev. 101, 2243-2270
4. Shabb, J. B. (2001) Physiological substrates of cAMP-dependent protein kinase. Chem. Rev. 101, 2381-2411
5. Kamenetsky, M., Middelhaufe, S., Bank, E. M., Levin, L. R., Buck, J., and Steegborn, C. (2006) Molecular details of cAMP generation in mammalian cells: a tale of two systems. J. Mol. Biol. 362, 623-639
6. Conti, M., and Beavo, J. (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu. Rev. Biochem. 76, 481-511
7. McKnight, G. S. (1991) Cyclic AMP second messenger systems. Curr. Opin. Cell Biol. 3, 213-217
8. Amieux, P. S., Cummings, D. E., Motamed, K., Brandon, E. P., Wailes, L. A., Le, K., Idzerda, R. L., and McKnight, G. S. (1997) Compensatory regulation of RIalpha protein levels in protein kinase A mutant mice. J. Biol. Chem. 272, 3993-3998
9. Amieux, P. S., and McKnight, G. S. (2002) The essential role of RI alpha in the maintenance of regulated PKA activity. Ann. N.Y. Acad. Sci. 968, 75-95
10. Wong, W., and Scott, J. D. (2004) AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell Biol. 5, 959-970
11. Baillie, G. S., Scott, J. D., and Houslay, M. D. (2005) Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett. 579, 3264-3270
12. Dodge, K. L., Khouangsathiene, S., Kapiloff, M. S., Mouton, R., Hill, E. V., Houslay, M. D., Langeberg, L. K., and Scott, J. D. (2001) mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. EMBO J. 20, 1921-1930
13. Gold, M. G., Lygren, B., Dokurno, P., Hoshi, N., McConnachie, G., Taskén, K., Carlson, C. R., Scott, J. D., and Barford, D. (2006) Molecular basis of AKAP specificity for PKA regulatory subunits. Mol. Cell 24, 383-395 (Pubitemid 44647900)
14. Burns, L. L., Canaves, J. M., Pennypacker, J. K., Blumenthal, D. K., and Taylor, S. S. (2003) Isoform specific differences in binding of a dual-specificity A-kinase anchoring protein to type I and type II regulatory subunits of PKA. Biochemistry 42, 5754-5763 (Pubitemid 36582867)
15. Huang, L. J., Wang, L., Ma, Y., Durick, K., Perkins, G., Deerinck, T. J., Ellisman, M. H., and Taylor, S. S. (1999) NH2-Terminal targeting motifs direct dual specificity A-kinase-anchoring protein 1 (D-AKAP1) to either mitochondria or endoplasmic reticulum. J. Cell Biol. 145, 951-959 (Pubitemid 29270054)
16. Han, P., Sonati, P., Rubin, C., and Michaeli, T. (2006) PDE7A1, a cAMP-specific phosphodiesterase, inhibits cAMP-dependent protein kinase by a direct interaction with C. J. Biol. Chem. 281, 15050-15057
17. Shaulsky, G., Fuller, D., and Loomis, W. F. (1998) A cAMP- phosphodiesterase controls PKA-dependent differentiation. Development 125, 691-699
18. Canaves, J. M., and Taylor, S. S. (2002) Classification and phylogenetic analysis of the cAMP-dependent protein kinase regulatory subunit family. J. Mol. Evol. 54, 17-29
19. Ogreid, D., and Døskeland, S. O. (1983) Cyclic nucleotides modulate the release of [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
20. Dao, K. K., Teigen, K., Kopperud, R., Hodneland, E., Schwede, F., Christensen, A. E., Martinez, A., and Døskeland, S. O. (2006) Epac1 and cAMP-dependent protein kinase holoenzyme have similar cAMP affinity, but their cAMP domains have distinct structural features and cyclic nucleotide recognition. J. Biol. Chem. 281, 21500-21511
21. Diller, T. C., Xuong, N. H., and Taylor, S. S. (2000) Type II beta regulatory subunit of cAMP-dependent protein kinase: purification strategies to optimize crystallization. Protein Expr. Purif. 20, 357-364
22. Anand, G., Taylor, S. S., and Johnson, D. A. (2007) Cyclic-AMP and Pseudosubstrate Effects on Type-I A-Kinase Regulatory and Catalytic Subunit Binding Kinetics. Biochemistry 46, 9283-9291
23. Herberg, F. W., Bell, S. M., and Taylor, S. S. (1993) Expression of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli: multiple isozymes reflect different phosphorylation states. Protein Eng. 6, 771-777 (Pubitemid 23293207)
24. Goodrich, J. A. a. K., J. F. (2007) Binding and kinetics for molecular biologists, 1st Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
25. Kool, J., van Marle, A., Hulscher, S., Selman, M., van Iperen, D. J., van Altena, K., Gillard, M., Bakker, R. A., Irth, H., Leurs, R., and Vermeulen, N. P. (2007) A flow-through fluorescence polarization detection system for measuring GPCR-mediated modulation of cAMP production. J. Biomol. Screen 12, 1074-1083 (Pubitemid 350179700)
26. Wales, T. E., Fadgen, K. E., Gerhardt, G. C., and Engen, J. R. (2008) High-speed and high-resolution UPLC separation at zero degrees Celsius. Anal. Chem. 80, 6815-6820
27. Bateman, R. H., Carruthers, R., Hoyes, J. B., Jones, C., Langridge, J. I., Millar, A., and Vissers, J. P. (2002) A novel precursor ion discovery method on a hybrid quadrupole orthogonal acceleration time-of-flight (Q-TOF) mass spectrometer for studying protein phosphorylation. J. Am. Soc. Mass Spectrom. 13, 792-803
28. Silva, J. C., Denny, R., Dorschel, C. A., Gorenstein, M., Kass, I. J., Li, G. Z., McKenna, T., Nold, M. J., Richardson, K., Young, P., and Geromanos, S. (2005) Quantitative proteomic analysis by accurate mass retention time pairs. Anal. Chem. 77, 2187-2200
29. Geromanos, S. J., Vissers, J. P., Silva, J. C., Dorschel, C. A., Li, G. Z., Gorenstein, M. V., Bateman, R. H., and Langridge, J. I. (2009) The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LC-MS/MS. Proteomics 9, 1683-1695
30. Li, G. Z., Vissers, J. P., Silva, J. C., Golick, D., Gorenstein, M. V., and Geromanos, S. J. (2009) Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures. Proteomics 9, 1696-1719
31. Weis, D. D., Engen, J. R., and Kass, I. J. (2006) Semi-automated data processing of hydrogen exchange mass spectra using HX-Express. J. Am. Soc. Mass Spectrom. 17, 1700-1703
32. Anand, G. S., Krishnamurthy, S., Bishnoi, T., Kornev, A., Taylor, S. S., and Johnson, D. A. (2010) Cyclic-AMP and Rp-cAMPS induced conformational changes in a complex of the catalytic and regulatory (RIa) subunits of PKA. Mol. Cell Proteomics oi:10.1074/mcp.M900388-MCP200.
33. Mandell, J. G., Falick, A. M., and Komives, E. A. (1998) Identification of protein-protein interfaces by decreased amide proton solvent accessibility. Proc. Natl. Acad. Sci. U.S.A. 95, 14705-14710
34. Kim, C., Xuong, N. H., and Taylor, S. S. (2005) Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA. Science 307, 690-696 (Pubitemid 40194632)
35. Su, Y., Dostmann, W. R., Herberg, F. W., Durick, K., Xuong, N. H., Ten Eyck, L., Taylor, S. S., and Varughese, K. I. (1995) Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains. Science 269, 807-813
36. Stock, A. M., Robinson, V. L., and Goudreau, P. N. (2000) Two-component signal transduction. Annu. Rev. Biochem. 69, 183-215
37. Thomason, P. A., Traynor, D., Cavet, G., Chang, W. T., Harwood, A. J., and Kay, R. R. (1998) An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium. EMBO J. 17, 2838-2845
38. Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2003) Protein analysis by hydrogen exchange mass spectrometry. Annu. Rev. Biophys. Biomol. Struct. 32, 1-25
39. Mandell, J. G., Baerga-Ortiz, A., Akashi, S., Takio, K., and Komives, E. A. (2001) Solvent accessibility of the thrombin-thrombomodulin interface. J. Mol. Biol. 306, 575-589
40. Anand, G. S., Hughes, C. A., Jones, J. M., Taylor, S. S., and Komives, E. A. (2002) Amide H/2H exchange reveals communication between the cAMP and catalytic subunit-binding sites in the R(I)alpha subunit of protein kinase A. J. Mol. Biol. 323, 377-386
41. Hughes, C. A., Mandell, J. G., Anand, G. S., Stock, A. M., and Komives, E. A. (2001) Phosphorylation causes subtle changes in solvent accessibility at the interdomain interface of methylesterase CheB. J. Mol. Biol. 307, 967-976
42. Cànaves, J. M., Leon, D. A., and Taylor, S. S. (2000) Consequences of cAMP-binding site mutations on the structural stability of the type I regulatory subunit of cAMP-dependent protein kinase. Biochemistry 39, 15022-15031
43. Wu, J., Jones, J. M., Nguyen-Huu, X., Ten Eyck, L. F., and Taylor, S. S. (2004) Crystal structures of RIalpha subunit of cyclic adenosine 5′-monophosphate (cAMP)-dependent protein kinase complexed with (Rp)-adenosine 3′,5′-cyclic monophosphothioate and (Sp)-adenosine 3′,5′-cyclic monophosphothioate, the phosphothioate analogues of cAMP. Biochemistry 43, 6620-6629 (Pubitemid 38697561)
44. Schwede, F., Christensen, A., Liauw, S., Hippe, T., Kopperud, R., Jastorff, B., and Døskeland, S. O. (2000) 8-Substituted cAMP analogues reveal marked differences in adaptability, hydrogen bonding, and charge accommodation between homologous binding sites (AI/AII and BI/BII) in cAMP kinase I and II. Biochemistry 39, 8803-8812
45. Kopperud, R., Christensen, A. E., Kjarland, E., Viste, K., Kleivdal, H., and Døskeland, S. O. (2002) Formation of inactive cAMP-saturated holoenzyme of cAMP-dependent protein kinase under physiological conditions. J. Biol. Chem. 277, 13443-13448
46. Corbin, J. D., Sugden, P. H., West, L., Flockhart, D. A., Lincoln, T. M., and McCarthy, D. (1978) Studies on the properties and mode of action of the purified regulatory subunit of bovine heart adenosine 3′:5′- monophosphate-dependent protein kinase. J. Biol. Chem. 253, 3997-4003 (Pubitemid 8361611)
47. Døskeland, S. O. (1978) Evidence that rabbit muscle protein kinase has two kinetically distinct binding sites for adenosine 3′; 5′-cyclic monophosphate. Biochem. Biophys. Res. Commun. 83, 542-549
48. Leiser, M., Fleischer, N., and Erlichman, J. (1986) Enhanced activation of cAMP-dependent protein kinase by rapid synthesis and degradation of cAMP. J. Biol. Chem. 261, 15486-15490
49. Diller, T. C., Madhusudan, Xuong, N. H., and Taylor, S. S. (2001) Molecular basis for regulatory subunit diversity in cAMP-dependent protein kinase: crystal structure of the type II beta regulatory subunit. Structure 9, 73-82 (Pubitemid 32064352)
50. Abu-Abed, M., Das, R., Wang, L., and Melacini, G. (2007) Definition of an electrostatic relay switch critical for the cAMP-dependent activation of protein kinase A as revealed by the D170A mutant of RIalpha. Proteins 69, 112-124 (Pubitemid 47339144)
51. Gibson, R. M., Ji-Buechler, Y., and Taylor, S. S. (1997) Interaction of the regulatory and catalytic subunits of cAMP-dependent protein kinase. Electrostatic sites on the type Ialpha regulatory subunit. J. Biol. Chem. 272, 16343-16350
52. Huang, L. J., and Taylor, S. S. (1998) Dissecting cAMP binding domain A in the RIalpha subunit of cAMP-dependent protein kinase. Distinct subsites for recognition of cAMP and the catalytic subunit. J. Biol. Chem. 273, 26739-26746