Phosphorylation of Cardiac Myosin-Binding Protein-C Is a Critical Mediator of Diastolic Function

Circulation: Heart Failure

Volumn 8, Issue 3, 2015, Pages 582-594

  Rosas, Paola C ^a   Liu, Yang ^a   Abdalla, Mohamed I ^a   Thomas, Candice M ^a   Kidwell, David T ^b   Dusio, Giuseppina F ^b   Mukhopadhyay, Dhriti ^b   Kumar, Rajesh ^a   Baker, Kenneth M ^a   Mitchell, Brett M ^a   Powers, Patricia A ^c   Fitzsimons, Daniel P ^c   Patel, Bindiya G ^d   Warren, Chad M ^d   Solaro, R John ^d   Moss, Richard L ^c   Tong, Carl W ^a,b  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

diastole; heart failure; myocardial contraction; myocardium; myosin binding protein C

Indexed keywords

BRAIN NATRIURETIC PEPTIDE; CALCIUM ION; MYOSIN BINDING PROTEIN C; CARRIER PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; MYOSIN-BINDING PROTEIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; ECHOCARDIOGRAPHY; FORCE; HEART CONTRACTION; HEART FAILURE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART PAPILLARY MUSCLE; IMMUNOFLUORESCENCE; MOUSE; MUSCLE RELAXATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RUNNING; SYSTOLIC BLOOD PRESSURE; TWO DIMENSIONAL GEL ELECTROPHORESIS; ANIMAL; BLOOD PRESSURE; COMPARATIVE STUDY; DIASTOLE; GENETICS; GENOTYPE; HEART LEFT VENTRICLE FUNCTION; KINETICS; METABOLISM; MUTATION; PATHOPHYSIOLOGY; PHENOTYPE; PHOSPHORYLATION; PROTEIN PROCESSING; TRANSGENIC MOUSE;

ANIMALS; BLOOD PRESSURE; CARRIER PROTEINS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIASTOLE; GENOTYPE; HEART FAILURE; KINETICS; MICE, TRANSGENIC; MUTATION; PHENOTYPE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT;

EID: 84934272453     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.114.001550     Document Type: Article

References (48)

1. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER 3rd, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation. 2014;129:e28-e292. doi: 10.1161/01. cir.0000441139.02102.80.
2. Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med. 2006;355:251-259. doi: 10.1056/NEJMoa052256.
3. McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Böhm M, Dickstein K, Falk V, Filippatos G, Fonseca C, Gomez-Sanchez MA, Jaarsma T, Køber L, Lip GY, Maggioni AP, Parkhomenko A, Pieske BM, Popescu BA, Rønnevik PK, Rutten FH, Schwitter J, Seferovic P, Stepinska J, Trindade PT, Voors AA, Zannad F, Zeiher A; ESC Committee for Practice Guidelines. ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: The Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association (HFA) of the ESC. Eur Heart J. 2012;33:1787-1847. doi: 10.1093/eurheartj/ehs104.
4. Redfield MM, Jacobsen SJ, Burnett JC Jr, Mahoney DW, Bailey KR, Rodeheffer RJ. Burden of systolic and diastolic ventricular dysfunction in the community: appreciating the scope of the heart failure epidemic. JAMA. 2003;289:194-202.
5. Offer G, Moos C, Starr R. A new protein of the thick filaments of vertebrate skeletal myofibrils. Extractions, purification and characterization. J Mol Biol. 1973;74:653-676.
6. Luther PK, Bennett PM, Knupp C, Craig R, Padrón R, Harris SP, Patel J, Moss RL. Understanding the organisation and role of myosin binding protein C in normal striated muscle by comparison with MyBP-C knockout cardiac muscle. J Mol Biol. 2008;384:60-72. doi: 10.1016/j. jmb.2008.09.013.
7. Gautel M, Zuffardi O, Freiburg A, Labeit S. Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: a modulator of cardiac contraction EMBO J. 1995;14:1952-1960.
8. Xiao L, Zhao Q, Du Y, Yuan C, Solaro RJ, Buttrick PM. PKCepsilon increases phosphorylation of the cardiac myosin binding protein C at serine 302 both in vitro and in vivo. Biochemistry. 2007;46:7054-7061. doi: 10.1021/bi700467k.
9. Dirkx E, Cazorla O, Schwenk RW, Lorenzen-Schmidt I, Sadayappan S, Van Lint J, Carrier L, van Eys GJ, Glatz JF, Luiken JJ. Protein kinase D increases maximal Ca2 +-activated tension of cardiomyocyte contraction by phosphorylation of cMyBP-C-Ser315. Am J Physiol Heart Circ Physiol. 2012;303:H323-H331. doi: 10.1152/ajpheart.00749.2011.
10. Schlender KK, Bean LJ. Phosphorylation of chicken cardiac C-protein by calcium/calmodulin-dependent protein kinase II. J Biol Chem. 1991;266:2811-2817.
11. Kuster DW, Sequeira V, Najafi A, Boontje NM, Wijnker PJ, Witjas-Paalberends ER, Marston SB, Dos Remedios CG, Carrier L, Demmers JA, Redwood C, Sadayappan S, van der Velden J. GSK3 phosphorylates newly identified site in the proline-alanine-rich region of cardiac myosin-binding protein C and alters cross-bridge cycling kinetics in human: short communication. Circ Res. 2013;112:633-639. doi: 10.1161/CIRCRESAHA.112.275602.
12. Cuello F, Bardswell SC, Haworth RS, Ehler E, Sadayappan S, Kentish JC, Avkiran M. Novel role for p90 ribosomal S6 kinase in the regulation of cardiac myofilament phosphorylation. J Biol Chem. 2011;286:5300-5310. doi: 10.1074/jbc.M110.202713.
13. Bardswell SC, Cuello F, Rowland AJ, Sadayappan S, Robbins J, Gautel M, Walker JW, Kentish JC, Avkiran M. Distinct sarcomeric substrates are responsible for protein kinase D-mediated regulation of cardiac myofilament Ca2 + sensitivity and cross-bridge cycling. J Biol Chem. 2010;285:5674-5682. doi: 10.1074/jbc.M109.066456.
14. Tong CW, Stelzer JE, Greaser ML, Powers PA, Moss RL. Acceleration of crossbridge kinetics by protein kinase A phosphorylation of cardiac myosin binding protein C modulates cardiac function. Circ Res. 2008;103:974-982. doi: 10.1161/CIRCRESAHA.108.177683.
15. Stelzer JE, Patel JR, Walker JW, Moss RL. Differential roles of cardiac myosin-binding protein C and cardiac troponin I in the myofibrillar force responses to protein kinase A phosphorylation. Circ Res. 2007;101: 503-511. doi: 10.1161/CIRCRESAHA.107.153650.
16. Coulton AT, Stelzer JE. Cardiac myosin binding protein C and its phosphorylation regulate multiple steps in the cross-bridge cycle of muscle contraction. Biochemistry. 2012;51:3292-3301. doi: 10.1021/bi300085x.
17. Tong CW, Nair NA, Doersch KM, Liu Y, Rosas PC. Cardiac myosinbinding protein-C is a critical mediator of diastolic function. Pflugers Arch. 2014;466:451-457. doi: 10.1007/s00424-014-1442-1.
18. Harris SP, Bartley CR, Hacker TA, McDonald KS, Douglas PS, Greaser ML, Powers PA, Moss RL. Hypertrophic cardiomyopathy in cardiac myosin binding protein-C knockout mice. Circ Res. 2002;90:594-601.
19. Layland J, Cave AC, Warren C, Grieve DJ, Sparks E, Kentish JC, Solaro RJ, Shah AM. Protection against endotoxemia-induced contractile dysfunction in mice with cardiac-specific expression of slow skeletal troponin I. FASEB J. 2005;19:1137-1139. doi: 10.1096/fj.04-2519fje.
20. Solaro RJ, Pang DC, Briggs FN. The purification of cardiac myofibrils with Triton X-100. Biochim Biophys Acta. 1971;245:259-262.
21. Scruggs SB, Hinken AC, Thawornkaiwong A, Robbins J, Walker LA, de Tombe PP, Geenen DL, Buttrick PM, Solaro RJ. Ablation of ventricular myosin regulatory light chain phosphorylation in mice causes cardiac dysfunction in situ and affects neighboring myofilament protein phosphorylation. J Biol Chem. 2009;284:5097-5106. doi: 10.1074/jbc. M807414200.
22. Warren CM, Arteaga GM, Rajan S, Ahmed RP, Wieczorek DF, Solaro RJ. Use of 2-D DIGE analysis reveals altered phosphorylation in a tropomyosin mutant (Glu54Lys) linked to dilated cardiomyopathy. Proteomics. 2008;8:100-105. doi: 10.1002/pmic.200700772.
23. Yuan C, Sheng Q, Tang H, Li Y, Zeng R, Solaro RJ. Quantitative comparison of sarcomeric phosphoproteomes of neonatal and adult rat hearts. Am J Physiol Heart Circ Physiol. 2008;295:H647-H656. doi: 10.1152/ajpheart.00357.2008.
24. Kirk JA, MacGowan GA, Evans C, Smith SH, Warren CM, Mamidi R, Chandra M, Stewart AF, Solaro RJ, Shroff SG. Left ventricular and myocardial function in mice expressing constitutively pseudophosphorylated cardiac troponin I. Circ Res. 2009;105:1232-1239. doi: 10.1161/CIRCRESAHA.109.205427.
25. Fritz JD, Swartz DR, Greaser ML. Factors affecting polyacrylamide gel electrophoresis and electroblotting of high-molecular-weight myofibrillar proteins. Anal Biochem. 1989;180:205-210.
26. Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure-abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med. 2004;350:1953-1959. doi: 10.1056/NEJMoa032566.
27. Tong CW, Gaffin RD, Zawieja DC, Muthuchamy M. Roles of phosphorylation of myosin binding protein-C and troponin I in mouse cardiac muscle twitch dynamics. J Physiol. 2004;558(Pt 3):927-941. doi: 10.1113/jphysiol.2004.062539.
28. Nagueh SF, Sun H, Kopelen HA, Middleton KJ, Khoury DS. Hemodynamic determinants of the mitral annulus diastolic velocities by tissue Doppler. J Am Coll Cardiol. 2001;37:278-285.
29. Seo JS, Kim DH, Kim WJ, Song JM, Kang DH, Song JK. Peak systolic velocity of mitral annular longitudinal movement measured by pulsed tissue Doppler imaging as an index of global left ventricular contractility. Am J Physiol Heart Circ Physiol. 2010;298:H1608-H1615. doi: 10.1152/ajpheart.01231.2009.
30. Ho CY, Solomon SD. A clinician's guide to tissue Doppler imaging. Circulation. 2006;113:e396-e398. doi: 10.1161/CIRCULATIONAHA. 105.579268.
31. Kasner M, Westermann D, Steendijk P, Gaub R, Wilkenshoff U, Weitmann K, Hoffmann W, Poller W, Schultheiss HP, Pauschinger M, Tschöpe C. Utility of Doppler echocardiography and tissue Doppler imaging in the estimation of diastolic function in heart failure with normal ejection fraction: a comparative Doppler-conductance catheterization study. Circulation. 2007;116:637-647. doi: 10.1161/CIRCULATIONAHA.106.661983.
32. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelista A. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr. 2009;22:107-133. doi: 10.1016/j.echo.2008.11.023.
33. Raff GL, Glantz SA. Volume loading slows left ventricular isovolumic relaxation rate. Evidence of load-dependent relaxation in the intact dog heart. Circ Res. 1981;48(6 Pt 1):813-824.
34. Previs MJ, Beck Previs S, Gulick J, Robbins J, Warshaw DM. Molecular mechanics of cardiac myosin-binding protein C in native thick filaments. Science. 2012;337:1215-1218. doi: 10.1126/science.1223602.
35. Colson BA, Rybakova IN, Prochniewicz E, Moss RL, Thomas DD. Cardiac myosin binding protein-C restricts intrafilament torsional dynamics of actin in a phosphorylation-dependent manner. Proc Natl Acad Sci USA. 2012;109:20437-20442. doi: 10.1073/pnas.1213027109.
36. Gruen M, Prinz H, Gautel M. CAPK-phosphorylation controls the interaction of the regulatory domain of cardiac myosin binding protein C with myosin-S2 in an on-off fashion. FEBS Lett. 1999;453:254-259.
37. Jeong EM, Monasky MM, Gu L, Taglieri DM, Patel BG, Liu H, Wang Q, Greener I, Dudley SC Jr, Solaro RJ. Tetrahydrobiopterin improves diastolic dysfunction by reversing changes in myofilament properties. J Mol Cell Cardiol. 2013;56:44-54. doi: 10.1016/j. yjmcc.2012.12.003.
38. Jin CZ, Jang JH, Kim HJ, Wang Y, Hwang IC, Sadayappan S, Park BM, Kim SH, Jin ZH, Seo EY, Kim KH, Kim YJ, Kim SJ, Zhang YH. Myofilament Ca2 + desensitization mediates positive lusitropic effect of neuronal nitric oxide synthase in left ventricular myocytes from murine hypertensive heart. J Mol Cell Cardiol. 2013;60:107-115. doi: 10.1016/j. yjmcc.2013.04.017.
39. Hamdani N, Bishu KG, von Frieling-Salewsky M, Redfield MM, Linke WA. Deranged myofilament phosphorylation and function in experimental heart failure with preserved ejection fraction. Cardiovasc Res. 2013;97:464-471. doi: 10.1093/cvr/cvs353.
40. Donaldson C, Palmer BM, Zile M, Maughan DW, Ikonomidis JS, Granzier H, Meyer M, VanBuren P, LeWinter MM. Myosin crossbridge dynamics in patients with hypertension and concentric left ventricular remodeling. Circ Heart Fail. 2012;5:803-811. doi: 10.1161/CIRCHEARTFAILURE.112.968925.
41. Copeland O, Sadayappan S, Messer AE, Steinen GJ, van der Velden J, Marston SB. Analysis of cardiac myosin binding protein-C phosphorylation in human heart muscle. J Mol Cell Cardiol. 2010;49:1003-1011. doi: 10.1016/j.yjmcc.2010.09.007.
42. van Dijk SJ, Paalberends ER, Najafi A, Michels M, Sadayappan S, Carrier L, Boontje NM, Kuster DW, van Slegtenhorst M, Dooijes D, dos Remedios C, ten Cate FJ, Stienen GJ, van der Velden J. Contractile dysfunction irrespective of the mutant protein in human hypertrophic cardiomyopathy with normal systolic function. Circ Heart Fail. 2012;5:36-46. doi: 10.1161/CIRCHEARTFAILURE.111.963702.
43. Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Drazner MH, Fonarow GC, Geraci SA, Horwich T, Januzzi JL, Johnson MR, Kasper EK, Levy WC, Masoudi FA, McBride PE, McMurray JJ, Mitchell JE, Peterson PN, Riegel B, Sam F, Stevenson LW, Tang WH, Tsai EJ, Wilkoff BL; WRITING COMMITTEE MEMBERS; American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on practice guidelines. Circulation. 2013;128:e240-e327. doi: 10.1161/CIR.0b013e31829e8776.
44. Zile MR, Gottdiener JS, Hetzel SJ, McMurray JJ, Komajda M, McKelvie R, Baicu CF, Massie BM, Carson PE; I-PRESERVE Investigators. Prevalence and significance of alterations in cardiac structure and function in patients with heart failure and a preserved ejection fraction. Circulation. 2011;124:2491-2501. doi: 10.1161/CIRCULATIONAHA.110.011031.
45. Kooij V, Holewinski RJ, Murphy AM, Van Eyk JE. Characterization of the cardiac myosin binding protein-C phosphoproteome in healthy and failing human hearts. J Mol Cell Cardiol. 2013;60:116-120. doi: 10.1016/j.yjmcc.2013.04.012.
46. Benovic JL, Mayor F Jr, Somers RL, Caron MG, Lefkowitz RJ. Lightdependent phosphorylation of rhodopsin by beta-adrenergic receptor kinase. Nature. 1986;321:869-872. doi: 10.1038/321869a0.
47. Zhu W, Petrashevskaya N, Ren S, Zhao A, Chakir K, Gao E, Chuprun JK, Wang Y, Talan M, Dorn GW 2nd, Lakatta EG, Koch WJ, Feldman AM, Xiao RP. Gi-biased 2AR signaling links GRK2 upregulation to heart failure. Circ Res. 2012;110:265-274. doi: 10.1161/CIRCRESAHA.111.253260.
48. Erickson JR, He BJ, Grumbach IM, Anderson ME. CaMKII in the cardiovascular system: sensing redox states. Physiol Rev. 2011;91:889-915. doi: 10.1152/physrev.00018.2010.