Cardiac resynchronization sensitizes the sarcomere to calcium by reactivating GSK-3?

Journal of Clinical Investigation

Volumn 124, Issue 1, 2014, Pages 129-139

  Kirk, Jonathan A ^a   Holewinski, Ronald J ^a   Kooij, Viola ^a   Agnetti, Giulio ^a,b   Tunin, Richard S ^a   Witayavanitkul, Namthip ^c   De Tombe, Pieter P ^c   Gao, Wei Dong ^d   Van Eyk, Jennifer ^a   Kass, David A ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHOPROTEIN PHOSPHATASE 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIAC RESYNCHRONIZATION THERAPY; CONTROLLED STUDY; DESENSITIZATION; DISEASE DURATION; DOG; ENZYME INACTIVATION; ENZYME REACTIVATION; HEART FAILURE; MASS SPECTROMETRY; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; SARCOMERE;

EID: 84892934846     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI69253     Document Type: Article

References (58)

1. Metra M, Bettari L, Carubelli V, Cas LD. Old and new intravenous inotropic agents in the treatment of advanced heart failure. Prog Cardiovasc Dis. 2011; 54(2):97-106.
2. Landmesser U, Drexler H. Update on inotropic therapy in the management of acute heart failure. Curr Treat Options Cardiovasc Med. 2007;9(6):443-449.
3. Kass DA, et al. Improved left ventricular mechanics from acute VDD pacing in patients with dilated cardiomyopathy and ventricular conduction delay. Circulation. 1999;99(12):1567-1573.
4. Nelson GS, et al. Left ventricular or biventricular pacing improves cardiac function at diminished energy cost in patients with dilated cardiomyopathy and left bundle-branch block. Circulation. 2000; 102(25):3053-3059.
5. Ukkonen H, et al. Effect of cardiac resynchronization on myocardial efficiency and regional oxidative metabolism. Circulation. 2003;107(1):28-31.
6. Cleland JG, et al. The effect of cardiac resynchronization on morbidity and mortality in heart failure. N Engl J Med. 2005;352(15):1539-1549.
7. Bristow MR, et al. Cardiac-resynchronization therapy with or without an implantable defibrillator in advanced chronic heart failure. N Engl J Med. 2004; 350(21):2140-2150.
8. Chalil S, et al. Intraventricular dyssynchrony predicts mortality and morbidity after cardiac resynchronization therapy: a study using cardiovascular magnetic resonance tissue synchronization imaging. J Am Coll Cardiol. 2007;50(3):243-252.
9. Gorcsan J 3rd, et al. Relationship of echocardiographic dyssynchrony to long-term survival after cardiac resynchronization therapy. Circulation. 2010; 122(19):1910-1918.
10. Barth AS, et al. Cardiac resynchronization therapy corrects dyssynchrony-induced regional gene expression changes on a genomic level. Circ Cardiovasc Genet. 2009;2(4):371-378.
11. Chakir K, et al. Reversal of global apoptosis and regional stress kinase activation by cardiac resynchronization. Circulation. 2008;117(11):1369-1377.
12. D'Ascia C, Cittadini A, Monti MG, Riccio G, Saccà L. Effects of biventricular pacing on interstitial remodelling, tumor necrosis factor-Alpha expression, and apoptotic death in failing human myocardium. Eur Heart J. 2006;27(2):201-206.
13. Nishijima Y, et al. Chronic cardiac resynchronization therapy and reverse ventricular remodeling in a model of nonischemic cardiomyopathy. Life Sci. 2007;81(14):1152-1159.
14. Mullens W, et al. Early and late effects of cardiac resynchronization therapy on force-frequency relation and contractility regulating gene expression in heart failure patients. Heart Rhythm. 2008;5(1):52-59.
15. Sachse FB, et al. Subcellular structures and function of myocytes impaired during heart failure are restored by cardiac resynchronization therapy. Circ Res. 2012;110(4):588-597.
16. Wang SB, Foster DB, Rucker J, O'Rourke B, Kass DA, Van Eyk JE. Redox regulation of mitochondrial ATP synthase: implications for cardiac resynchronization therapy. Circ Res. 2011;109(7):750-757.
17. Aiba T, et al. Electrophysioloigcal consequences of dyssynchronous heart failure and its restoration by resynchronization therapy. Circulation. 2009; 119(9):1220-1230.
18. Aiba T, Tomaselli G. Electrical remodeling in dyssynchrony and resynchronization. J Cardiovasc Transl Re. 2012;5(2):170-179.
19. Chakir K, et al. Galphas-biased ®2-Adrenergic receptor signaling from restoring synchronous contraction in the failing heart. Sci Transl Med. 2011; 3(100):100ra188.
20. Chakir K, et al. Mechanisms of enhanced betaadrenergic reserve from cardiac resynchronization therapy. Circulation. 2009;119(9):1231-1240.
21. Malik FI, et al. Cardiac myosin activation: a potential therapeutic approach for systolic heart failure. Science. 2011;331(6023):1439-1443.
22. Sorsa T, Pollesello P, Solaro RJ. The contractile apparatus as a target for drugs against heart failure: interaction of levosimendan, a calcium sensitiser, with cardiac troponin c. Mol Cell Biochem. 2004; 266(1-2):87-107.
23. Cleland JG, et al. The effects of the cardiac myosin activator, omecamtiv mecarbil, on cardiac function in systolic heart failure: a double-blind, placebocontrolled, crossover, dose-ranging phase 2 trial. Lancet. 2011;378(9792):676-683.
24. Belin RJ, et al. Augmented protein kinase C-Alphainduced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ Res. 2007; 101(2):195-204.
25. Kooij V, et al. Protein kinase C alpha and epsilon phosphorylation of troponin and myosin binding protein C reduce Ca2+ sensitivity in human myocardium. Basic Res Cardiol. 2010;105(2):289-300.
26. Solaro RJ, van der Velden J. Why does troponin I have so many phosphorylation sites? Fact and fancy. J Mol Cell Cardiol. 2010;48(5):810-816.
27. Murphy AM, et al. Transgenic mouse model of stunned myocardium. Science. 2000; 287(5452):488-491.
28. Nassar R, et al. cTnT1, a cardiac troponin T isoform, decreases myofilament tension and affects the left ventricular pressure waveform. Am J Physiol Heart Circ Physiol. 2005;288(3):H1147-H1156.
29. Pi Y, Zhang D, Kemnitz KR, Wang H, Walker JW. Protein kinase C and A sites on troponin I regulate myofilament Ca2+ sensitivity and ATPase activity in the mouse myocardium. J Physiol. 2003; 552(pt 3):845-857.
30. Burkart EM, et al. Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J Biol Chem. 2003; 278(13):11265-11272.
31. Kirk JA, et al. Left ventricular and myocardial function in mice expressing constitutively pseudophosphorylated cardiac troponin I. Circ Res. 2009; 105(12):1232-1239.
32. Wang H, Grant JE, Doede CM, Sadayappan S, Robbins J, Walker JW. PKC-®⊃⊃ sensitizes cardiac myofilaments to Ca2+ by phosphorylating troponin I on threonine-144. J Mol Cell Cardiol. 2006;41(5):823-833.
33. Nixon BR, et al. AMP-Activated protein kinase phosphorylates cardiac troponin I at Ser-150 to increase myofilament calcium sensitivity and blunt PKA-dependent function. J Biol Chem. 2012; 287(23):19136-19147.
34. Buscemi N, Foster DB, Neverova I, Van Eyk JE. p21-Activated kinase increases the calcium sensitivity of rat triton-skinned cardiac muscle fiber bundles via a mechanism potentially involving novel phosphorylation of troponin I. Circ Res. 2002; 91(6):509-516.
35. Chen PP, Patel JR, Rybakova IN, Walker JW, Moss RL. Protein kinase A-induced myofilament desensitization to Ca(2+) as a result of phosphorylation of cardiac myosin-binding protein C. J Gen Physiol. 2010;136(6):615-627.
36. Sadayappan S, et al. A critical function for Ser- 282 in cardiac Myosin binding protein-C phosphorylation and cardiac function. Circ Res. 2011; 109(2):141-150.
37. van der Velden J, et al. The effect of myosin light chain 2 dephosphorylation on Ca2+ -sensitivity of force is enhanced in failing human hearts. Cardiovasc Res. 2003;57(2):505-514.
38. Sumandea MP, Pyle WG, Kobayashi T, de Tombe PP, Solaro RJ. Identification of a functionally critical protein kinase C phosphorylation residue of cardiac troponin T. J Biol Chem. 2003; 278(37):35135-35144.
39. Vahebi S, Kobayashi T, Warren CM, de Tombe PP, Solaro RJ. Functional effects of rho-kinase-dependent phosphorylation of specific sites on cardiac troponin. Circ Res. 2005;96(7):740-747.
40. Wolff MR, Buck SH, Stoker SW, Greaser ML, Mentzer RM. Myofibrillar calcium sensitivity of isometric tension is increased in human dilated cardiomyopathies: role of altered beta-Adrenergically mediated protein phosphorylation. J Clin Invest. 1996;98(1):167-176.
41. Marston SB, de Tombe PP. Troponin phosphorylation and myofilament Ca2+-sensitivity in heart failure: increased or decreased? J Mol Cell Cardiol. 2008; 45(5):603-607.
42. Cho GY, et al. Mechanical dyssynchrony assessed by tissue Doppler imaging is a powerful predictor of mortality in congestive heart failure with normal QRS duration. J Am Coll. 2005;46(12):2237-2243.
43. Kashani A, Barold SS. Significance of QRS complex duration in patients with heart failure. J Am Coll Cardiol. 2005;46(12):2183-2192.
44. Vanagt WY, et al. Pacing-induced dys-synchrony preconditions rabbit myocardium against ischemia/reperfusion injury. Circulation. 2006; 114(1 suppl):I264-I269.
45. van Berlo JH, Maillet M, Molkentin JD. Signaling effectors underlying pathologic growth and remodeling of the heart. J Clin Invest. 2013;123(1):37-45.
46. Ambardekar AV, et al. Incomplete recovery of myocyte contractile function despite improvement of myocardial architecture with left ventricular assist device support. Circ Heart Fail. 2011; 4(4):425-432.
47. Fan D, Wannenburg T, de Tombe PP. Decreased myocyte tension development and calcium responsiveness in rat right ventricular pressure overload. Circulation. 1997;95(9):2312-2317.
48. Zhang P, et al. Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart. Circulation. 2012; 126(15):1828-1837.
49. Pyle WG, Hart MC, Cooper JA, Sumandea MP, de Tombe PP, Solaro RJ. Actin capping protein: an essential element in protein kinase signaling to the myofilaments. Circ Res. 2002;90(12):1299-1306.
50. Gupta MP, Samant SA, Smith SH, Shroff SG. HDAC4 and PCAF bind to cardiac sarcomeres and play a role in regulating myofilament contractile activity. J Biol Chem. 2008;283(15):10135-10146.
51. Ponomareva EV, Ogneva IV. [Contractile properties, transversal stiffness and cytoskeletal protein content in Mongolian gerbils soleus fibers under long-term hindlimb suspension]. Biofizika. 2012; 57(4):683-689.
52. Hassel D, et al. Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nat Med. 2009;15(11):1281-1288.
53. Kimura A. Molecular basis of hereditary cardiomyopathy: abnormalities in calcium sensitivity, stretch response, stress response and beyond. J Hum Genet. 2010;55(2):81-90.
54. Kuster DW, et al. GSK3® phosphorylates newly identified site in the proline-Alanine-rich region of cardiac myosin-binding protein C and alters crossbridge cycling kinetics in human: short communication. Circ Res. 2013;112(4):633-639.
55. Kovacic-Milivojevic B, Roediger F, Almeida EA, Damsky CH, Gardner DG, Ilic D. Focal adhesion kinase and p130Cas mediate both sarcomeric organization and activation of genes associated with cardiac myocyte hypertrophy. Mol Biol Cell. 2001; 12(8):2290-2307.
56. Kong SW, et al. Heart failure-Associated changes in RNA splicing of sarcomere genes. Circ Cardiovasc Genet. 2010;3(2):138-146.
57. Roof DJ, Hayes A, Adamian M, Chishti AH, Li T. Molecular characterization of abLIM, a novel actinbinding and double zinc finger protein. J Cell Biol. 1997;138(3):575-588.
58. Liu CP, Ting CT, Lawrence W, Maughan WL, Chang MS, Kass DA. Diminished contractile response to increased heart rate in intact human left ventricular hypertrophy. Systolic versus diastolic determinants. Circulation. 1993;88(4 pt 1):1893-1906.