Troponin I phosphorylation in human myocardium in health and disease

Netherlands Heart Journal

Volumn 22, Issue 10, 2014, Pages 463-469

  Wijnker, P J M ^a,b   Murphy, A M ^c   Stienen, G J M ^a,d   van der Velden, J ^a,e  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

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

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

Author keywords

Cardiac troponin I; Heart failure; Myofilament function; Phosphorylation

Indexed keywords

BETA ADRENERGIC RECEPTOR; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE C; TROPONIN I;

ARTICLE; HEART DISEASE; HEART FAILURE; HEART LEFT VENTRICLE FILLING; HEART MUSCLE; HEART PERFORMANCE; HUMAN; HYPERTROPHY; MYOFILAMENT; NONHUMAN; PROTEIN PHOSPHORYLATION; STARLING LAW;

EID: 84908040879     PISSN: 15685888     EISSN: 18766250     Source Type: Journal    
DOI: 10.1007/s12471-014-0590-4     Document Type: Article

References (48)

1. Thygesen K, Mair J, Katus H, et al. Study group on biomarkers in cardiology of the ESC working group on acute cardiac care. Recommendations for the use of cardiac troponin measurement in acute cardiac care. Eur Heart J. 2010;31:2197-204.
2. Newby LK, Jesse RL, Babb JD, et al. ACCF 2012 expert consensus document on practical clinical considerations in the interpretation of troponin elevations: a report of the american college of cardiology foundation task force on clinical expert consensus documents. J Am Coll Cardiol. 2012;60:2427-63.
3. Barta J, Tóth A, Edes I, et al. Calpain-1-sensitive myofibrillar proteins of the human myocardium. Mol Cell Biochem. 2005;278:1-8.
4. Kobayashi T, Solaro RJ. Calcium, thin filaments, and the integrative biology of cardiac contractility. Annu Rev Physiol. 2005;67:39-67.
5. Lehman W, Craig R. Tropomyosin and the steric mechanism of muscle regulation. Adv Exp Med Biol. 2008;644:95-109.
6. Zhang P, Kirk JA, JiW, et al.Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart. Circulation. 2012;126:1828-37.
7. Solaro RJ, Henze M, Kobayashi T. Integration of troponin I phosphorylation with cardiac regulatory networks. Circ Res. 2013;112: 355-66.
8. Solaro RJ, van der Velden J. Why does troponin I have so many phosphorylation sites? fact and fancy. J Mol Cell Cardiol. 2010;48: 810-6.
9. van der Velden J. Diastolic myofilament dysfunction in the failing human heart. Pflugers Arch. 2011;462:155-63.
10. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415: 198-205.
11. Solaro RJ, Moir AJ, Perry SV. Phosphorylation of troponin I and the inotropic effect of adrenaline in the perfused rabbit heart. Nature. 1976;262:615-7.
12. Takimoto E, Soergel DG, Janssen PM, Stull LB, Kass DA, Murphy AM. Frequency- and afterload-dependent cardiac modulation in vivo by troponin I with constitutively active protein kinase a phosphorylation sites. Circ Res. 2004;94:496-504.
13. Swiderek K, Jaquet K, Meyer HE, Schachtele C, Hofmann F, Heilmeyer Jr LM. Sites phosphorylated in bovine cardiac troponin T and I. Characterization by 31P-NMR spectroscopy and phosphorylation by protein kinases. Eur J Biochem. 1990;190: 575-82.
14. Haworth RS, Cuello F, Herron TJ, et al. Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ Res. 2004;95:1091-9.
15. Blumenthal DK, Stull JT, Gill GN. Phosphorylation of cardiac troponin by guanosine 3′:5′-monophosphate-dependent protein kinase. J Biol Chem. 1978;253:324-6.
16. Jideama NM, Crawford BH, Hussain AK, Raynor RL. Dephosphorylation specificities of protein phosphatase for cardiac troponin I, troponin T, and sites within troponin T. Int J Biol Sci. 2006;2:1-9.
17. Deshmukh PA, Blunt BC, Hofmann PA. Acute modulation of PP2a and troponin I phosphorylation in ventricular myocytes: studies with a novel PP2a peptide inhibitor. Am J Physiol Heart Circ Physiol. 2007;292:H792-799.
18. Wijnker PJM, Boknik P, Gergs U, et al. Protein phosphatase 2A affects myofilament contractility in non-failing but not in failing human myocardium. J Muscle Res Cell Motil. 2011;32:221-33.
19. Hamdani N, Borbely A, Veenstra SP, et al. More severe cellular phenotype in human idiopathic dilated cardiomyopathy compared to ischemic heart disease. J Muscle Res Cell Motil. 2010;31: 289-301.
20. 2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc Res. 2003;57:37-47.
21. Zhang J, Guy MJ, Norman HS, et al. Top-down quantitative proteomics identified phosphorylation of cardiac troponin I as a candidate biomarker for chronic heart failure. J Proteome Res. 2011;10: 4054-65.
22. Zabrouskov V, Ge Y, Schwartz J, Walker JW. Unraveling molecular complexity of phosphorylated human cardiac troponin I by top down electron capture dissociation/electron transfer dissociation mass spectrometry. Mol Cell Proteomics. 2008;7:1838-49.
23. 2+ affinity of cardiac troponin C. J Biol Chem. 1995;270:30773-80.
24. Wijnker PJM, Foster DB, Tsao AL, et al. Impact of site-specific phosphorylation of protein kinase A sites Ser23 and Ser24 of cardiac troponin I in human cardiomyocytes. Am J Physiol Heart Circ Physiol. 2013;304:H260-8.
25. van der Velden J, Klein LJ, Zaremba R, et al. Effects of calcium, inorganic phosphate, and pH on isometric force in single skinned cardiomyocytes from donor and failing human hearts. Circulation. 2001;104:1140-6.
26. van Dijk SJ, Paalberends ER, Najafi A, et al. Contractile dysfunction irrespective of the mutant protein in human hypertrophic cardiomyopathy with normal systolic function. Circ Heart Fail. 2012;5:36-46.
27. Messer AE, Gallon CE, McKenna WJ, Dos Remedios CG, Marston SB. The use of phosphate-affinity SDS-PAGE to measure the cardiac troponin I phosphorylation site distribution in human heart muscle. Proteomics Clin Appl. 2009;3:1371-82.
28. van Dijk SJ, Dooijes D, Dos Remedios CG, et al. Cardiac myosinbinding protein C mutations and hypertrophic cardiomyopathy: haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation. 2009;119:1473-83.
29. de Tombe PP, Mateja RD, Tachampa K, Ait MY, Farman GP, Irving TC. Myofilament length dependent activation. J Mol Cell Cardiol. 2010;48:851-8.
30. 2+ activation in cardiac muscle: some remaining questions. J Muscle Res Cell Motil. 2005;26:199-212.
31. Arteaga GM, Palmiter KA, Leiden JM, Solaro RJ. Attenuation of length dependence of calcium activation in myofilaments of transgenic mouse hearts expressing slow skeletal troponin I. J Physiol. 2000;526:541-9.
32. Konhilas JP, Irving TC, Wolska BM, et al. Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing. J Physiol. 2003;547:951-61.
33. Wijnker PJM, Sequeira V, Foster DB, et al. Length-dependent activation is modulated by cardiac troponin I bisphosphorylation at Ser23 and Ser24 but not by Thr143 phosphorylation. Am J Physiol Heart Circ Physiol. 2014;306:H1171-1181.
34. Schwinger RH, Bohm M, Koch A, et al. The failing human heart is unable to use the Frank-Starling mechanism. Circ Res. 1994;74:959-69.
35. 2+-sensitive isoforms in the failing human heart. Circulation. 1999;99:384-91.
36. Noland Jr TA, Raynor RL, Kuo JF. Identification of sites phosphorylated in bovine cardiac troponin I and troponin T by protein kinase C and comparative substrate activity of synthetic peptides containing the phosphorylation sites. J Biol Chem. 1989;264:20778-85.
37. Sumandea MP, Burkart EM, Kobayashi T, De Tombe PP, Solaro RJ. Molecular and integrated biology of thin filament protein phosphorylation in heart muscle. Ann N YAcad Sci. 2004;1015:39-52.
38. Burkart EM, Sumandea MP, Kobayashi T, 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;278:11265-72.
39. 2+ sensitivity in human myocardium. Basic Res Cardiol. 2010;105:289-300.
40. van der Velden J, Narolska NA, Lamberts RR, et al. Functional effects of protein kinase C-mediated myofilament phosphorylation in human myocardium. Cardiovasc Res. 2006;69:876-87.
41. 2+-sensitivity and blunts enhanced length-dependent activation in response to protein kinase A in human cardiomyocytes. Arch Biochem Biophys. 2014;554:11-21.
42. Fabiato A. Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calciuminduced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle. J Gen Physiol. 1981;78:457-97.
43. 2+ by phosphorylating troponin I on threonine-144. J Mol Cell Cardiol. 2006;41:823-33.
44. Tachampa K,Wang H, Farman GP, de Tombe PP. Cardiac troponin I threonine 144: role in myofilament length dependent activation. Circ Res. 2007;101:1081-3.
45. Kitzman DW, Higginbotham MB, Cobb FR, Sheikh KH, Sullivan MJ. Exercise intolerance in patients with heart failure and preserved left ventricular systolic function: failure of the Frank-Starling mechanism. J Am Coll Cardiol. 1991;17:1065-72.
46. Ross Jr J, Braunwald E. Studies on Starling's law of the heart. IX. The effects of impeding venous return on performance of the normal and failing human left ventricle. Circulation. 1964;30:719-27.
47. Sequeira V, Wijnker PJM, Nijenkamp LL, et al. Perturbed lengthdependent activation in human hypertrophic cardiomyopathy with missense sarcomeric gene mutations. Circ Res. 2013;112: 1491-505.
48. Lang SE, Robinson DA,Wu HC, Herron TJ,Wahr PA,Westfall MV. Myofilament incorporation and contractile function after gene transfer of cardiac troponin I Ser43/45Ala. Arch Biochem Biophys. 2013;535:49-55.