Active site coupling in PDE:PKA complexes promotes resetting of mammalian cAMP signaling

Biophysical Journal

Volumn 107, Issue 6, 2014, Pages 1426-1440

  Krishnamurthy, Srinath ^a,b   Moorthy, Balakrishnan Shenbaga ^a   Xiang, Lim Xin ^a   Shan, Lim Xin ^a   Bharatham, Kavitha ^c   Tulsian, Nikhil Kumar ^a   Mihalek, Ivana ^c   Anand, Ganesh S ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c BIOINFORMATICS INSTITUTE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; CYCLIC AMP PHOSPHODIESTERASE; PDE8A PROTEIN, HUMAN;

CHEMISTRY; ENZYME ACTIVE SITE; HUMAN; METABOLISM; MOLECULAR DOCKING; NUCLEOTIDE SEQUENCE; SIGNAL TRANSDUCTION;

3',5'-CYCLIC-AMP PHOSPHODIESTERASES; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIALPHA SUBUNIT; HUMANS; MOLECULAR DOCKING SIMULATION; SIGNAL TRANSDUCTION;

EID: 84909580096     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.07.050     Document Type: Article

References (77)

1. Rehmann, H., A. Rueppel, ..., A. Wittinghofer. 2003. Communication between the regulatory and the catalytic region of the cAMP-responsive guanine nucleotide exchange factor Epac. J. Biol. Chem. 278:23508-23514.
2. Kamenetsky, M., S. Middelhaufe, ..., C. Steegborn. 2006. Molecular details of cAMP generation in mammalian cells: a tale of two systems. J. Mol. Biol. 362:623-639.
3. Conti, M., and J. Beavo. 2007. Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu. Rev. Biochem. 76:481-511.
4. Rich, T. C., K. A. Fagan, ..., J. W. Karpen. 2001. A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc. Natl. Acad. Sci. USA. 98:13049-13054.
5. Steinberg, S. F., and L. L. Brunton. 2001. Compartmentation of G protein-coupled signaling pathways in cardiac myocytes. Annu. Rev. Pharmacol. Toxicol. 41:751-773.
6. Baillie, G. S., D. R. Adams, ..., M. D. Houslay. 2007. Mapping binding sites for the PDE4D5 cAMP-specific phosphodiesterase to the N- and C-domains of β-arrestin using spot-immobilized peptide arrays. Biochem. J. 404:71-80.
7. 2+-triggered membrane association with selectivity for interaction with phosphatidic acid. J. Biol. Chem. 277:28298-28309.
8. Bolger, G. B., G. S. Baillie, ..., M. D. Houslay. 2006. Scanning peptide array analyses identify overlapping binding sites for the signaling scaffold proteins, β-arrestin and RACK1, in cAMP-specific phosphodiesterase PDE4D5. Biochem. J. 398:23-36.
9. 2+. J. Cell Sci. 119:3799-3810.
10. 1H NMR structural and functional characterization of a cAMP-specific phosphodiesterase-4D5 (PDE4D5) N-terminal region peptide that disrupts PDE4D5 interaction with the signaling scaffold proteins, β-arrestin and RACK1. Cell. Signal. 19:2612-2624.
11. Houslay, M. D. 2010. Underpinning compartmentalized cAMP signaling through targeted cAMP breakdown. Trends Biochem. Sci. 35:91-100.
12. Houslay, M. D., G. S. Baillie, and D. H. Maurice. 2007. cAMP-specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ. Res. 100:950-966.
13. Keravis, T., and C. Lugnier. 2010. Cyclic nucleotide phosphodiesterases (PDE) and peptide motifs. Curr. Pharm. Des. 16:1114-1125.
14. 2+ channel Cav1.2. Science. 293:98-101.
15. Berman, H. M., L. F. Ten Eyck, ..., S. S. Taylor. 2005. The cAMP binding domain: an ancient signaling module. Proc. Natl. Acad. Sci. USA. 102:45-50.
16. Taylor, S. S., C. Kim, ..., G. S. Anand. 2005. Dynamics of signaling by PKA. Biochim. Biophys. Acta. 1754:25-37.
17. Das, R., V. Esposito, ..., G. Melacini. 2007. cAMP activation of PKA defines an ancient signaling mechanism. Proc. Natl. Acad. Sci. USA. 104:93-98.
18. Johnson, D. A., P. Akamine, ..., S. S. Taylor. 2001. Dynamics of cAMP-dependent protein kinase. Chem. Rev. 101:2243-2270.
19. Kim, C., C. Y. Cheng, ..., S. S. Taylor. 2007. PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation. Cell. 130:1032-1043.
20. Kim, C., N. H. Xuong, and S. S. Taylor. 2005. Crystal structure of a complex between the catalytic and regulatory (RIa) subunits of PKA. Science. 307:690-696.
21. Su, Y., W. R. Dostmann, ..., K. I. Varughese. 1995. Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains. Science. 269:807-813.
22. Abu-Abed, M., R. Das, ..., G. Melacini. 2007. Definition of an electrostatic relay switch critical for the cAMP-dependent activation of protein kinase A as revealed by the D170A mutant of RIα. Proteins. 69:112-124.
23. Byeon, I. J., K. K. Dao, ..., A. M. Gronenborn. 2010. Allosteric communication between cAMP binding sites in the RI subunit of protein kinase A revealed by NMR. J. Biol. Chem. 285:14062-14070.
24. Das, R., M. Abu-Abed, and G. Melacini. 2006. Mapping allostery through equilibrium perturbation NMR spectroscopy. J. Am. Chem. Soc. 128:8406-8407.
25. Das, R., S. Chowdhury, ..., G. Melacini. 2009. Dynamically driven ligand selectivity in cyclic nucleotide binding domains. J. Biol. Chem. 284:23682-23696.
26. Das, R., M. T. Mazhab-Jafari, ..., G. Melacini. 2008. Entropy-driven cAMP-dependent allosteric control of inhibitory interactions in exchange proteins directly activated by cAMP. J. Biol. Chem. 283:19691-19703.
27. Das, R., and G. Melacini. 2007. A model for agonism and antagonism in an ancient and ubiquitous cAMP-binding domain. J. Biol. Chem. 282:581-593.
28. McNicholl, E. T., R. Das, ..., G. Melacini. 2010. Communication between tandem cAMP binding domains in the regulatory subunit of protein kinase A-Iα as revealed by domain-silencing mutations. J. Biol. Chem. 285:15523-15537.
29. Anand, G. S., M. Hotchko, ..., S. S. Taylor. 2007. R-subunit isoform specificity in protein kinase A: distinct features of protein interfaces in PKA types I and II by amide H/2H exchange mass spectrometry. J. Mol. Biol. 374:487-499.
30. Anand, G. S., C. A. Hughes, ..., E. A. Komives. 2002. Amide H/2H exchange reveals communication between the cAMP and catalytic subunit-binding sites in the RIα subunit of protein kinase A. J. Mol. Biol. 323:377-386.
31. Hamuro, Y., G. S. Anand, ..., V. L. Woods, Jr. 2004. Mapping intersubunit interactions of the regulatory subunit (RIα) in the type I holoenzyme of protein kinase A by amide hydrogen/deuterium exchange mass spectrometry (DXMS). J. Mol. Biol. 340:1185-1196.
32. Anand, G. S., S. Krishnamurthy, ..., D. A. Johnson. 2010. Cyclic AMP- and (Rp)-cAMP-induced conformational changes in a complex of the catalytic and regulatory (RIα) subunits of cyclic AMP-dependent protein kinase. Mol. Cell. Proteomics. 9:2225-2237.
33. Badireddy, S., G. Yunfeng, ..., G. S. Anand. 2011. Cyclic AMP analog blocks kinase activation by stabilizing inactive conformation: conformational selection highlights a new concept in allosteric inhibitor design. Mol. Cell. Proteomics. 10: M110-004390.
34. Boehr, D. D., R. Nussinov, and P. E. Wright. 2009. The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5:789-796.
35. Changeux, J. P. 2012. Allostery and the Monod-Wyman-Changeux model after 50 years. Annu. Rev. Biophys. 41:103-133.
36. Moorthy, B. S., S. Badireddy, and G. S. Anand. 2011. Cooperativity and allostery in cAMP-dependent activation of protein kinase A: monitoring conformations of intermediates by amide hydrogen/deuterium exchange. Int. J. Mass Spectrom. 302:157-166.
37. Herberg, F. W., W. R. Dostmann, ..., S. S. Taylor. 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.
38. Moorthy, B. S., Y. Gao, and G. S. Anand. 2011. Phosphodiesterases catalyze hydrolysis of cAMP-bound to regulatory subunit of protein kinase A and mediate signal termination. Mol. Cell. Proteomics. 10:M110-002295.
39. Shaulsky, G., D. Fuller, and W. F. Loomis. 1998. A cAMP-phosphodiesterase controls PKA-dependent differentiation. Development. 125:691-699.
40. Krishnamurthy, S., B. S. Moorthy, ..., G. S. Anand. 2013. Dynamics of phosphodiesterase-induced cAMP dissociation from protein kinase A: capturing transient ternary complexes by HDXMS. Biochim. Biophys. Acta. 1834:1215-1221.
41. Corbin, J. D., P. H. Sugden, ..., D. McCarthy. 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.
42. 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.
43. Dodge, K. L., S. Khouangsathiene, ..., J. D. Scott. 2001. mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. EMBO J. 20:1921-1930.
44. 16. Biochem. J. 446:437-443.
45. Lynch, M. J., G. S. Baillie, ..., M. D. Houslay. 2005. RNA silencing identifies PDE4D5 as the functionally relevant cAMP phosphodiesterase interacting with β arrestin to control the protein kinase A/AKAP79-mediated switching of the β2-adrenergic receptor to activation of ERK in HEK293B2 cells. J. Biol. Chem. 280:33178-33189.
46. McCahill, A., T. McSorley, ..., M. D. Houslay. 2005. In resting COS1 cells a dominant negative approach shows that specific, anchored PDE4 cAMP phosphodiesterase isoforms gate the activation, by basal cyclic AMP production, of AKAP-tethered protein kinase A type II located in the centrosomal region. Cell. Signal. 17:1158-1173.
47. Anand, G. S., D. Law, ..., E. A. Komives. 2003. Identification of the protein kinase A regulatory RIα-catalytic subunit interface by amide H/2H exchange and protein docking. Proc. Natl. Acad. Sci. USA. 100:13264-13269.
48. Pandit, D., S. J. Tuske, ..., Y. Hamuro. 2012. Mapping of discontinuous conformational epitopes by amide hydrogen/deuterium exchange mass spectrometry and computational docking. J. Mol. Rec. 25:114-124.
49. Roberts, V. A., M. E. Pique, ..., V. L.Woods, Jr. 2012. Combining H/D exchange mass spectroscopy and computational docking reveals extended DNA-binding surface on uracil-DNA glycosylase. Nucleic Acids Res. 40:6070-6081.
50. Yan, Z., H. Wang, ..., H. Ke. 2009. Refolding and kinetic characterization of the phosphodiesterase-8A catalytic domain. Protein Expr. Purif. 64:82-88.
51. Diller, T. C., N. H. Xuong, and S. S. Taylor. 2000. Type II β-regulatory subunit of cAMP-dependent protein kinase: purification strategies to optimize crystallization. Protein Expr. Purif. 20:357-364.
52. Anand, G., S. S. Taylor, and D. A. Johnson. 2007. Cyclic-AMP and pseudosubstrate effects on type-I A-kinase regulatory and catalytic subunit binding kinetics. Biochemistry. 46:9283-9291.
53. Buechler, Y. J., and S. S. Taylor. 1991. Mutations in the autoinhibitor site of the regulatory subunit of cAMP-dependent protein kinase I. Replacement of Ala-97 and Ser-99 interferes with reassociation with the catalytic subunit. J. Biol. Chem. 266:3491-3497.
54. Wales, T. E., K. E. Fadgen, ..., J. R. Engen. 2008. High-speed and high-resolution UPLC separation at zero degrees Celsius. Anal. Chem. 80:6815-6820.
55. Bateman, R. H., R. Carruthers, ..., J. P. Vissers. 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.
56. Silva, J. C., R. Denny, ..., S. Geromanos. 2005. Quantitative proteomic analysis by accurate mass retention time pairs. Anal. Chem. 77:2187-2200.
57. Geromanos, S. J., J. P. Vissers, ..., J. I. Langridge. 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.
58. Shen, Z., P. Li, ..., B. C. Wang. 2009. Label-free quantitative proteomics analysis of etiolated maize seedling leaves during greening. Mol. Cell. Proteomics. 8:2443-2460.
59. Dominguez, C., R. Boelens, and A. M. Bonvin. 2003. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125:1731-1737.
60. Arnold, K., L. Bordoli, ..., T. Schwede. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modeling. Bioinformatics. 22:195-201.
61. Wang, H., Z. Yan, ..., H. Ke. 2008. Kinetic and structural studies of phosphodiesterase-8A and implication on the inhibitor selectivity. Biochemistry. 47:12760-12768.
62. Thomason, P. A., D. Traynor, ..., R. R. Kay. 1998. An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium. EMBO J. 17:2838-2845.
63. Poppe, H., S. D. Rybalkin, ..., E. Butt. 2008. Cyclic nucleotide analogs as probes of signaling pathways. Nat. Methods. 5:277-278.
64. Akimoto, M., R. Selvaratnam, ..., G. Melacini. 2013. Signaling through dynamic linkers as revealed by PKA. Proc. Natl. Acad. Sci. USA. 110:14231-14236.
65. Kornev, A. P., S. S. Taylor, and L. F. Ten Eyck. 2008. A generalized allosteric mechanism for cis-regulated cyclic nucleotide binding domains. PLOS Comput. Biol. 4:e1000056.
66. Selvaratnam, R., S. Chowdhury, ..., G. Melacini. 2011. Mapping allostery through the covariance analysis of NMR chemical shifts. Proc. Natl. Acad. Sci. USA. 108:6133-6138.
67. Lensink, M. F., and S. J.Wodak. 2010. Docking and scoring protein interactions: CAPRI 2009. Proteins. 78:3073-3084.
68. Brown, K. M., J. P. Day, ..., G. S. Baillie. 2013. Phosphodiesterase-8A binds to and regulates Raf-1 kinase. Proc. Natl. Acad. Sci. USA. 110:E1533-E1542.
69. Huang, X., H. M. Holden, and F. M. Raushel. 2001. Channeling of substrates and intermediates in enzyme-catalyzed reactions. Annu. Rev. Biochem. 70:149-180.
70. Leiser, M., N. Fleischer, and J. Erlichman. 1986. Enhanced activation of cAMP-dependent protein kinase by rapid synthesis and degradation of cAMP. J. Biol. Chem. 261:15486-15490.
71. Burns-Hamuro, L. L., Y. Ma, ..., S. S. Taylor. 2003. Designing isoform-specific peptide disruptors of protein kinase A localization. Proc. Natl. Acad. Sci. USA. 100:4072-4077.
72. Sathyanarayana, P., E. Houde, ..., D. M. Wojchowski. 2009. CNTO 530 functions as a potent EPO mimetic via unique sustained effects on bone marrow proerythroblast pools. Blood. 113:4955-4962.
73. Bogacheva, O., O. Bogachev, ..., D. M. Wojchowski. 2008. DYRK3 dual-specificity kinase attenuates erythropoiesis during anemia. J. Biol. Chem. 283:36665-36675.
74. Mandell, J. G., A. Baerga-Ortiz, ..., E. A. Komives. 2001. Solvent accessibility of the thrombin-thrombomodulin interface. J. Mol. Biol. 306:575-589.
75. Houde, D., S. A. Berkowitz, and J. R. Engen. 2011. The utility of hydrogen/deuterium exchange mass spectrometry in biopharmaceutical comparability studies. J. Pharm. Sci. 100:2071-2086.
76. Wojchowski, D. M., M. P. Menon, ..., O. Bogachev. 2006. Erythropoietin-dependent erythropoiesis: new insights and questions. Blood Cells Mol. Dis. 36:232-238.
77. Pikitch, E. K., C. Santora, ..., K. J. Sainsbury. 2004. Ecology. Ecosystem-based fishery management. Science. 305:346-347.