Contractile dysfunction irrespective of the mutant protein in human hypertrophic cardiomyopathy with normal systolic function

Circulation: Heart Failure

Volumn 5, Issue 1, 2012, Pages 36-46

  Van Dijk, Sabine J ^a   Paalberends, E Rosalie ^a   Najafi, Aref ^a   Michels, Michelle ^c   Sadayappan, Sakthivel ^d   Carrier, Lucie ^e   Boontje, Nicky M ^a   Kuster, Diederik W D ^a   Van Slegtenhorst, Marjon ^a   Dooijes, Dennis ^f   Dos Remedios, Cris ^g   Cate, Folkert J ^c   Stienen, Ger J M ^a,b   Van Der Velden, Jolanda ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d LOYOLA UNIVERSITY CHICAGO   (United States)

^e University Medical   (Germany)

^f Utrecht Medical Center   (Netherlands)

^g UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cardiomyopathy; Mutation; Myocardial contraction; Myofilament proteins

Indexed keywords

CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; MUTANT PROTEIN; MYOSIN BINDING PROTEIN C; TROPONIN I; CALCIUM; CARRIER PROTEIN; MYOSIN-BINDING PROTEIN C;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DISEASE COURSE; FEMALE; GENE; GENE MUTATION; HAPLOINSUFFICIENCY; HEART CONTRACTION; HEART LEFT VENTRICLE CONTRACTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILE FORCE; HUMAN; HUMAN TISSUE; HYPERTROPHIC CARDIOMYOPATHY; MALE; MYBPC3 GENE; MYOFILAMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SARCOMERE; SARCOMERE LENGTH; BLOOD PRESSURE; COMPARATIVE STUDY; DIASTOLE; DRUG EFFECT; GENETICS; HEART LEFT VENTRICLE FUNCTION; MIDDLE AGED; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SYSTOLE;

ADULT; AGED; BLOOD PRESSURE; CALCIUM; CARDIOMYOPATHY, HYPERTROPHIC; CARRIER PROTEINS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIASTOLE; DISEASE PROGRESSION; FEMALE; HUMANS; MALE; MIDDLE AGED; MUTATION; MYOCARDIAL CONTRACTION; PHOSPHORYLATION; SARCOMERES; SYSTOLE; VENTRICULAR FUNCTION, LEFT;

EID: 84859632282     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.111.963702     Document Type: Article

References (48)

1. Alcalai R, Seidman JG, Seidman CE. Genetic basis of hypertrophic cardiomyopathy: From bench to the clinics. J Cardiovasc Electrophysiol. 2008;19:104-110.
2. Richard P, Charron P, Carrier L, Ledeuil C, Cheav T, Pichereau C, Benaiche A, Isnard R, Dubourg O, Burban M, Gueffet JP, Millaire A, Desnos M, Schwartz K, Hainque B, Komajda M. Hypertrophic cardiomyopathy: Distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation. 2003;107:2227-2232. (Pubitemid 36547217)
3. Wang L, Seidman JG, Seidman CE. Narrative review: Harnessing molecular genetics for the diagnosis and management of hypertrophic cardiomyopathy. Ann Intern Med. 2010;152:513-520.
4. Carrier L, Schlossarek S, Willis MS, Eschenhagen T. The ubiquitinproteasome system and nonsense-mediated mRNA decay in hypertrophic cardiomyopathy. Cardiovasc Res. 2010;85:330-338.
5. Ramaraj R. Hypertrophic cardiomyopathy: Etiology, diagnosis, and treatment. Cardiol Rev. 2008;16:172-180.
6. Ho CY, Carlsen C, Thune JJ, Havndrup O, Bundgaard H, Farrohi F, Rivero J, Cirino AL, Andersen PS, Christiansen M, Maron BJ, Orav EJ, Kober L. Echocardiographic strain imaging to assess early and late consequences of sarcomere mutations in hypertrophic cardiomyopathy. Circ Cardiovasc Genet. 2009;2:314-321.
7. Gandjbakhch E, Gackowski A, Tezenas du MS, Isnard R, Hamroun A, Richard P, Komajda M, Charron P. Early identification of mutation carriers in familial hypertrophic cardiomyopathy by combined echocardiography and tissue Doppler imaging. Eur Heart J. 2010;31:1599-1607.
8. Germans T, Russel IK, Gotte MJ, Spreeuwenberg MD, Doevendans PA, Pinto YM, van der Geest RJ, van der Velden J, Wilde AA, van Rossum AC. How do hypertrophic cardiomyopathy mutations affect myocardial function in carriers with normal wall thickness? Assessment with cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2010;12:13.
9. Michels M, Soliman OI, Kofflard MJ, Hoedemaekers YM, Dooijes D, Majoor-Krakauer D, Ten Cate FJ. Diastolic abnormalities as the first feature of hypertrophic cardiomyopathy in Dutch myosin-binding protein C founder mutations. J Am Coll Cardiol Cardiovasc Imaging. 2009;2:58-64.
10. Germans T, Wilde AA, Dijkmans PA, Chai W, Kamp O, Pinto YM, van Rossum AC. Structural abnormalities of the inferoseptal left ventricular wall detected by cardiac magnetic resonance imaging in carriers of hypertrophic cardiomyopathy mutations. J Am Coll Cardiol. 2006;48:2518-2523. (Pubitemid 44881223)
11. Ho CY, Lopez B, Coelho-Filho OR, Lakdawala NK, Cirino AL, Jarolim P, Kwong R, Gonzalez A, Colan SD, Seidman JG, Diez J, Seidman CE. Myocardial fibrosis as an early manifestation of hypertrophic cardiomyopathy. N Engl J Med. 2010;363:552-563.
12. van Dijk SJ, Dooijes D, dos Remedios C, Michels M, Lamers JM, Winegrad S, Schlossarek S, Carrier L, Ten Cate FJ, Stienen GJM, van der Velden J. Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy: Haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation. 2009;119:1473-1483.
13. Marston S, Copeland O, Jacques A, Livesey K, Tsang V, McKenna WJ, Jalilzadeh S, Carballo S, Redwood C, Watkins H. Evidence from human myectomy samples that MYBPC3 mutations cause hypertrophic cardiomyopathy through haploinsufficiency. Circ Res. 2009;105:219-222.
14. Hershberger RE, Cowan J, Morales A, Siegfried JD. Progress with genetic cardiomyopathies: Screening, counseling, and testing in dilated, hypertrophic, and arrhythmogenic right ventricular dysplasia/cardiomyopathy. Circ Heart Fail. 2009;2:253-261.
15. Zaremba R, Merkus D, Hamdani N, Lamers JMJ, Paulus WJ, dos Remedios C, Duncker DJ, Stienen GJM, van der Velden J. Quantitative analysis of myofilament protein phosphorylation in small cardiac biopsies. Proteom Clin Appl. 2007;1:1285-1290.
16. El Armouche A, Pohlmann L, Schlossarek S, Starbatty J, Yeh YH, Nattel S, Dobrev D, Eschenhagen T, Carrier L. Decreased phosphorylation levels of cardiac myosin-binding protein-C in human and experimental heart failure. J Mol Cell Cardiol. 2007;43:223-229. (Pubitemid 47079047)
17. Copeland O, Sadayappan S, Messer AE, Stienen 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.
18. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T. Phosphatebinding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics. 2006;5:749-757.
19. Kooij V, Saes M, Jaquet K, Zaremba R, Foster DB, Murphy AM, dos Remedios C, van der Velden J, Stienen GJM. Effect of troponin I Ser23/24 phosphorylation on Ca2-sensitivity in human myocardium depends on the phosphorylation background. J Mol Cell Cardiol. 2010;48:954-963.
20. Messer AE, Gallon CE, McKenna WJ, dos Remedios C, Marston SB. The use of phosphate-affinity SDS-PAGE to measure the cardiac troponin I phosphorylation site distribution in human heart muscle. Proteom Clin Appl. 2009;3:1371-1382.
21. van der Velden J, Papp Z, Zaremba R, Boontje NM, de Jong JW, Owen VJ, Burton PB, Goldmann P, Jaquet K, Stienen GJM. Increased Ca2- sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc Res. 2003;57:37-47. (Pubitemid 36009434)
22. Shub C, Klein AL, Zachariah PK, Bailey KR, Tajik AJ. Determination of left ventricular mass by echocardiography in a normal population: Effect of age and sex in addition to body size. Mayo Clin Proc. 1994;69:205-211. (Pubitemid 24085951)
23. Maron BJ, McKenna WJ, Danielson GK, Kappenberger LJ, Kuhn HJ, Seidman CE, Shah PM, Spencer WH, III, Spirito P, Ten Cate FJ, Wigle ED. American College of Cardiology/European Society of Cardiology clinical expert consensus document on hypertrophic cardiomyopathy. A report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents and the European Society of Cardiology Committee for Practice Guidelines. J Am Coll Cardiol. 2003;42:1687-1713. (Pubitemid 37383745)
24. Decker RS, Decker ML, Kulikovskaya I, Nakamura S, Lee DC, Harris K, Klocke FJ, Winegrad S. Myosin-binding protein C phosphorylation, myofibril structure, and contractile function during low-flow ischemia. Circulation. 2005;111:906-912. (Pubitemid 40279893)
25. Sadayappan S, Osinska H, Klevitsky R, Lorenz JN, Sargent M, Molkentin JD, Seidman CE, Seidman JG, Robbins J. Cardiac myosin binding protein C phosphorylation is cardioprotective. Proc Natl Acad Sci U S A. 2006; 103:16918-16923. (Pubitemid 44737353)
26. Olivotto I, Girolami F, Ackerman MJ, Nistri S, Bos JM, Zachara E, Ommen SR, Theis JL, Vaubel RA, Re F, Armentano C, Poggesi C, Torricelli F, Cecchi F. Myofilament protein gene mutation screening and outcome of patients with hypertrophic cardiomyopathy. Mayo Clin Proc. 2008;83: 630-638. (Pubitemid 351810562)
27. 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. (Pubitemid 34640910)
28. Carrier L, Knoll R, Vignier N, Keller DI, Bausero P, Prudhon B, Isnard R, Ambroisine ML, Fiszman M, Ross J Jr, Schwartz K, Chien KR. Asymmetric septal hypertrophy in heterozygous cMyBP-C null mice. Cardiovasc Res. 2004;63:293-304. (Pubitemid 38900843)
29. Messer AE, Jacques AM, Marston SB. Troponin phosphorylation and regulatory function in human heart muscle: Dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J Mol Cell Cardiol. 2007;42:247-259. (Pubitemid 44970468)
30. Hamdani N, Kooij V, van Dijk S, Merkus D, Paulus WJ, dos Remedios C, Duncker DJ, Stienen GJM, van der Velden J. Sarcomeric dysfunction in heart failure. Cardiovasc Res. 2008;77:649-658. (Pubitemid 351301859)
31. Hamdani N, Borbely A, Veenstra SP, Kooij V, Vrydag W, Zaremba R, dos Remedios C, Niessen HW, Michel MC, Paulus WJ, Stienen GJM, van der Velden J. More severe cellular phenotype in human idiopathic dilated cardiomyopathy compared to ischemic heart disease. J Muscle Res Cell Motil. 2010;31:289-301.
32. El Armouche A, and Eschenhagen T. Beta-adrenergic stimulation and myocardial function in the failing heart. Heart Fail Rev. 2009;14:225-241.
33. 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.
34. Mohamed AS, Dignam JD, Schlender KK. Cardiac myosin-binding protein C (MyBP-C): Identification of protein kinase A and protein kinase C phosphorylation sites. Arch Biochem Biophys. 1998;358:313-319. (Pubitemid 28480950)
35. Sadayappan S, Gulick J, Martin LA, Cuello F, Avkiran M, Lorenz JN, Robbins J. Hierarchical an critical functions of Ser282 phosphorylation in cardiac myosin binding protein-C phosphorylation and cardiac function. Circulation. 2009;120:S870. Abstract.
36. Tong CW, Wu X, Sadayappan S, Hudmon A, Muthuchamy M, Ralphe JC, Valdivia HH, Moss RL. Frequency dependent phosphorylation of cardiac myosin binding protein-C mediates acceleration of myocardial relaxation to support normal diastolic function. Circulation. 2009;122: A16507. Abstract.
37. Hoskins AC, Jacques A, Bardswell SC, McKenna WJ, Tsang V, dos Remedios CG, Ehler E, Adams K, Jalilzadeh S, Avkiran M, Watkins H, Redwood C, Marston SB, Kentish JC. Normal passive viscoelasticity but abnormal myofibrillar force generation in human hypertrophic cardiomyopathy. J Mol Cell Cardiol. 2010;49:737-745.
38. Borbely A, van der Velden J, Papp Z, Bronzwaer JG, Edes I, Stienen GJM, Paulus WJ. Cardiomyocyte stiffness in diastolic heart failure. Circulation. 2005;111:774-781. (Pubitemid 40250638)
39. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415:198-205. (Pubitemid 34059525)
40. Cazorla O, Szilagyi S, Vignier N, Salazar G, Kramer E, Vassort G, Carrier L, Lacampagne A. Length and protein kinase A modulations of myocytes in cardiac myosin binding protein C-deficient mice. Cardiovasc Res. 2006;69:370-380. (Pubitemid 43098793)
41. Kooij V, Boontje N, Zaremba R, Jaquet K, dos Remedios C, Stienen GJ, van der Velden J. Protein kinase C alpha and epsilon phosphorylation of troponin and myosin binding protein C reduce Ca2-sensitivity in human myocardium. Basic Res Cardiol. 2010;105:289-300.
42. Chen PP, Patel JR, Rybakova IN, Walker JW, Moss RL. Protein kinase A-induced myofilament desensitization to Ca2 as a result of phosphorylation of cardiac myosin-binding protein C. J Gen Physiol. 2010;136:615-627.
43. Hofmann PA, Hartzell HC, Moss RL. Alterations in Ca2 sensitive tension due to partial extraction of C-protein from rat skinned cardiac myocytes and rabbit skeletal muscle fibers. J Gen Physiol. 1991;97:1141-1163.
44. Konhilas JP, Irving TC, de Tombe PP. Frank-Starling law of the heart and the cellular mechanisms of length-dependent activation. Pflugers Arch. 2002;445:305-310. (Pubitemid 35452539)
45. Hanft LM, Korte FS, McDonald KS. Cardiac function and modulation of sarcomeric function by length. Cardiovasc Res. 2008;77:627-636. (Pubitemid 351301873)
46. Konhilas JP, Irving TC, Wolska BM, Jweied EE, Martin AF, Solaro RJ, de Tombe PP. Troponin I in the murine myocardium: Influence on lengthdependent activation and interfilament spacing. J Physiol. 2003;547: 951-961. (Pubitemid 36367375)
47. Duncker DJ, Boontje NM, Merkus D, Versteilen A, Krysiak J, Mearini G, El Armouche A, de Beer VJ, Lamers JM, Carrier L, Walker LA, Linke WA, Stienen GJM, van der Velden J. Prevention of myofilament dysfunction by beta-blocker therapy in postinfarct remodeling. Circ Heart Fail. 2009;2:233-242.
48. Hamdani N, Paulus WJ, van Heerebeek L, Borbely A, Boontje NM, Zuidwijk MJ, Bronzwaer JG, Simonides WS, Niessen HW, Stienen GJM, van der Velden J. Distinct myocardial effects of beta-blocker therapy in heart failure with normal and reduced left ventricular ejection fraction. Eur Heart J. 2009;30:1863-1872.