Ser-2030, but not Ser-2808, is the major phosphorylation site in cardiac ryanodine receptors responding to protein kinase A activation upon β-adrenergic stimulation in normal and failing hearts

Biochemical Journal

Volumn 396, Issue 1, 2006, Pages 7-16

  Xiao, Bailong ^a   Zhong, Guofeng ^a   Obayashi, Masakazu ^a   Yang, Dongmei ^b   Chen, Keyun ^a   Walsh, Michael P ^c   Shimoni, Yakhin ^a   Cheng, Heping ^b   Keurs, Henk Ter ^a   Chen, S R Wayne ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

adrenergic stimulation; Heart failure (HF); Phospho specific antibodies; Protein kinase A (PKA); Ryanodine receptor (RyR) phosphorylation

Indexed keywords

ANTIBODIES; CARDIOVASCULAR SYSTEM; CHEMICAL ACTIVATION; PHYSIOLOGY; PROTEINS; STOICHIOMETRY;

Β-ADRENERGIC STIMULATION; HEART FAILURE (HF); PHOSPHO-SPECIFIC ANTIBODIES; PROTEIN KINASE A (PKA); RYANODINE RECEPTOR (RYR) PHOSPHORYLATION;

ENZYME KINETICS;

CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOPRENALINE; PROTEIN SUBUNIT; RYANODINE RECEPTOR; SERINE;

ANIMAL CELL; ARTICLE; BETA ADRENERGIC STIMULATION; CONTROLLED STUDY; HEART FAILURE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL;

ADRENERGIC BETA-AGONISTS; ANIMALS; ARRHYTHMIA; BENZYLAMINES; BLOTTING, WESTERN; CALCIUM SIGNALING; CARRIER PROTEINS; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HEART FAILURE, CONGESTIVE; HUMANS; ION CHANNEL GATING; ION TRANSPORT; ISOPROTERENOL; KIDNEY; MICE; MYOCYTES, CARDIAC; OXAZOLES; PEPTIDE FRAGMENTS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; RABBITS; RATS; RECOMBINANT FUSION PROTEINS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SODIUM-CALCIUM EXCHANGER; STAUROSPORINE; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONAMIDES; TRANSFECTION;

EID: 33646771721     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060116     Document Type: Article

References (32)

1. Bers, D. M. (2002) Cardiac excitation-contraction coupling. Nature (London) 415, 198-205
2. Bean, B., Nowycky, M. and Tsien, R. (1984) Beta-adrenergic modulation of calcium channels in frog ventricular heart cells. Nature (London) 307, 371-375
3. Yue, D., Herzig, S. and Marban, E. (1990) Beta-adrenergic stimulation of calcium channels occurs by potentiation of high-activity gating modes. Proc. Natl. Acad. Sci. U.S.A. 87, 753-757
4. MacLennan, D. and Kranias, E. (2003) Phospholamban: a crucial regulator of cardiac contractility. Nat. Rev. Mol. Cell Biol. 4, 566-577
5. Bers, D. M., Eisner, D. A. and Valdivia, H. H. (2003) Sarcoplasmic reticulum Ca2+ and heart failure: roles of diastolic leak and Ca2+ transport. Circ. Res. 93, 487-490
6. Marx, S. O., Reiken, S., Hisamatsu, Y., Jayaraman, T., Burkhoff, D., Rosemblit, N. and Marks, A. R. (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101, 365-376
7. Wehrens, X. H. T., Lehnart, S. E., Reiken, S. R. and Marks, A. R. (2004) Ca2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ. Res. 94, 61-70
8. Witcher, D. R., Kovacs, R. J., Schulman, H., Cefali, D, C. and Jones, L. R. (1991) Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J. Biol. Chem. 266, 11144-11152
9. Witcher, D. R., Strifler, B. A. and Jones, L. R. (1992) Cardiac-specific phosphorylation site for multifunctional Ca2+/calmodulin-dependent protein kinase is conserved in the brain ryanodine receptor. J. Biol. Chem. 267, 4963-4967
10. Lehnart, S., Wehrens, X., Reiken, S., Warrier, S., Belevych, A., Harvey, R., Richter, W., Jin, S., Conti, M. and Marks, A. (2005) Phosphodiesterase 4D deficiency in the ryanodine-receptor complex promotes heart failure and arrhythmias. Cell 123, 25-35
11. Wehrens, X., Lehnart, S., Reiken, S., Vest, J., Wronska, A. and Marks, A. (2006) Ryanodine receptor/calcium release channel PKA phosphorylation: a critical mediator of heart failure progression. Proc. Natl. Acad. Sci. U.S.A. 103, 511-518
12. Takasago, T., Imagawa, T., Furukawa, K., Ogurusu, T. and Shigekawa, M. (1991) Regulation of the cardiac ryanodine receptor by protein kinase-dependent phosphorylation. J. Biochem. (Tokyo) 109, 163-170
13. Xiao, B., Jiang, M. T., Zhao, M., Yang, D., Sutherland, C., Lai, F. A., Walsh, M. P., Warltier, D. C., Cheng, H. and Chen, S. R. W. (2005) Characterization of a novel PKA phosphorylation site, serine-2030, reveals no PKA hyperphosphorytation of the cardiac ryanodine receptor in canine heart failure. Circ. Res. 96, 847-855
14. Reiken, S., Gaburjakova, M., Guatimosim, S., Gomez, A. M., D'Armiento, J., Burkhoff, D., Wang, J., Vassort, G., Lederer, W. J. and Marks, A. R. (2003) Protein kinase A phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. Role of phosphatases and response to isoproterenol. J. Biol. Chem. 278, 444-453
15. Jiang, M. T., Lokuta, A. J., Farrell, E. F., Wolff, M. R., Haworth, R. A. and Valdivia, H. H. (2002) Abnormal Ca2+ release, but normal ryanodine receptors, in canine and human heart failure. Circ. Res. 91, 1015-1022
16. Stange, M., Xu, L., Balshaw, D., Yamaguchi, N. and Meissner, G. (2003) Characterization of recombinant skeletal muscle (Ser-2843) and cardiac muscle (Ser-2809) ryanodine receptor phosphorylation mutants. J. Biol. Chem. 278, 51693-51702
17. Rodriguez, P., Bhogal, M. S. and Colyer, J. (2003) Stoichiometric phosphorylation of cardiac ryanodine receptor on serine-2809 by calmodulin-dependent kinase II and protein kinase A. J. Biol. Chem. 278, 38593-38600
18. Xiao, B., Sutherland, C., Walsh, M. P. and Chen, S. R. W. (2004) Protein kinase A phosphorylation at serine-2808 of the cardiac Ca2+-release channel (ryanodine receptor) does not dissociate 12.6-kDa FK506-binding protein (FKBP12.6). Circ. Res. 94, 487-495
19. Demaille, J. G., Peters, K. A., Strandjord, T. P. and Fischer, E. H. (1978) Isolation and properties of the bovine brain protein inhibitor of adenosine 3′:5′-monophosphate-dependent protein kinases. FEBS Lett. 86, 113-116
20. Zhao, M., Li, P., Li, X., Zhang, L., Winkfein, R. J. and Chen, S. R. (1999) Molecular identification of the ryanodine receptor pore-forming segment. J. Biol. Chem. 274, 25971-25974
21. Li, P. and Chen, S. R. (2001) Molecular basis of Ca2+ activation of the mouse cardiac Ca2+ release channel (ryanodine receptor). J. Gen. Physiol. 118, 33-44
22. Zhu, W.-Z., Wang, S.-Q., Chakir, K., Yang, D., Zhang, T., Brown, J. H., Devic, E., Kobilka, B. K., Cheng, H. and Xiao, R.-P. (2003) Linkage of β1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+/calmodulin kinase II. J. Clin. Invest. 111, 617-625
23. Obayashi, M., Xiao, B., Stuyvers, B., Davidoff, A., Mei, J., Chen, S. and ter Keurs, H. (2006) Spontaneous diastolic contractions and phosphorylation of the cardiac ryanodine receptor at serine-2808 in congestive heart failure in rat. Cardiovasc Res. 69, 140-151
24. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227, 680-685
25. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76, 4350-4354
26. Kennelly, P. and Krebs, E. (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266, 15555-15558
27. Vest, J. A., Wehrens, X. H. T., Reiken, S. R., Lehnart, S. E., Dobrev, D., Chandra, P., Danilo, P., Ravens, U., Rosen, M. R. and Marks, AR. (2005) Detective cardiac ryanodine receptor regulation during atrial fibrillation. Circulation 111, 2025-2032
28. Oda, T., Yano, M., Yamamoto, T., Tokuhisa, T., Okuda, S., Doi, M., Ohkusa, T., Ikeda, Y., Kobayashi, S., Ikemoto, N. and Matsuzaki, M. (2005) Defective regulation of interdomain interactions within the ryanodine receptor plays a key role in the pathogenesis of heart failure. Circulation 111, 3400-3410
29. Wang, W., Zhu, W., Wang, S., Yang, D., Crow, M. T., Xiao, R.-P. and Cheng, H. (2004) Sustained β1-adrenergic stimulation modulates cardiac contractility by Ca2+/calmodulin kinase signaling pathway. Circ Res. 95, 798-806
30. Zhang, T., Maier, L. S., Dalton, N. D., Miyamoto, S., Ross, Jr, J., Bers, D. M. and Brown, J. H. (2003) The {delta}c isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ Res. 92, 912-919
31. Ai, X., Curran, J. W., Shannon, T. R., Bers, D. M. and Pogwizd, S. M. (2005) Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ. Res. 97, 1314-1322
32. Pogwizd, S. M., Schlotthauer, K., Li, L., Yuan, W. and Bers, D. M. (2001) Arrhythmogenesis and contractile dysfunction in heart failure: roles of sodium-calcium exchange, inward rectifier potassium current, and residual β-adrenergic responsiveness. Circ Res. 88, 1159-1167