Regulation of cardiac contractile function by troponin I phosphorylation

Cardiovascular Research

Volumn 66, Issue 1, 2005, Pages 12-21

  Layland, Joanne ^a   Solaro, R John ^b   Shah, Ajay M ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Myocardial contractility; Phosphorylation; Protein kinases; Troponin I

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1; ENDOTHELIN A RECEPTOR AGONIST; MUTANT PROTEIN; PHENYLEPHRINE; PHOSPHOPROTEIN PHOSPHATASE; SERINE; THREONINE; TROPONIN; TROPONIN C;

CALCIUM CELL LEVEL; DEPHOSPHORYLATION; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE HYPERTROPHY; HUMAN; IN VITRO STUDY; INFORMATION; MUSCLE RELAXATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SEPSIS; THIN FILAMENT;

ANIMALS; CALCIUM; HEART FAILURE, CONGESTIVE; HUMANS; MICE; MICE, TRANSGENIC; MICROFILAMENTS; MODELS, ANIMAL; MYOCARDIAL CONTRACTION; MYOCARDIUM; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; TROPONIN I;

EID: 14844344027     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2004.12.022     Document Type: Review

References (92)

1. R.J. Solaro Modulation of cardiac myofilament activity by protein phosphorylation E. Page H. Fozzard R.J. Solaro Handbook of physiology 2001 Oxford University Press New York 264 300
2. R.J. Solaro, and H.M. Rarick Troponin and tropomyosin. Proteins that switch on and tune in the activity of cardiac myofilaments Circ. Res. 83 1998 471 480
3. P.M.L. Janssen, L.B. Stull, and E. Marban Myofilament properties comprise the rate-limiting step for cardiac relaxation at body temperature in the rat Am. J. Physiol. 282 2002 H499 H507
4. T. Noguchi, M. Hunlich, P.C. Camp, K.J. Begin, M. El-Zaru, and R. Patten Thin filament-based modulation of contractile performance in human heart failure Circulation 110 2004 982 987
5. J.M. Metzger, and M.V. Westfall Covalent and noncovalent modification of thin filament action. The essential role of troponin in cardiac muscle regulation Circ. Res. 94 2004 146 158
6. G.S. Bodor, A.E. Oakeley, P.D. Allen, D.L. Ladenson, and P.A. Anderson Troponin I phosphorylation in the normal and failing adult human heart Circulation 96 1997 1495 1500
7. D.R. Zakhary, C.S. Moravec, R.W. Stewart, and M. Bond Protein kinase A (PKA)-dependent troponin-I phosphorylation and PKA regulatory subunits are decreased in human dilated cardiomyopathy Circulation 99 1999 505 510
8. 2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins Cardiovasc. Res. 57 2003 37 47
9. J.F.Y. Hoh, G.H. Rossmanith, L.J. Kwan, and A.M. Hamilton Adrenaline increases the rate of cycling of crossbridges in rat cardiac muscle as measured by pseudo-random binary noise-modulated perturbation analysis Circ. Res. 62 1988 452 461
10. Y. Saeki, K. Shiozawa, K. Yanagisawa, and T. Shibata Adrenaline increases the rate of cross-bridge cycling in rat cardiac muscle J. Mol. Cell. Cardiol. 22 1990 453 460
11. K.T. Strang, N.K. Sweitzer, M.L. Greaser, and R.L. Moss β-Adrenergic receptor stimulation increases unloaded shortening velocity of skinned single ventricular myocytes from rats Circ. Res. 74 1994 542 549
12. R. Zhang, J. Zhao, A. Mandveno, and J.D. Potter Cardiac troponin-I phosphorylation increases the rate of cardiac muscle relaxation Circ. Res. 76 1995 1028 1035
13. R.C. Fentzke, S.H. Buck, J.R. Patel, H. Lin, B.M. Wolska, and M.O. Stojanovic Impaired cardiomyocyte relaxation and diastolic function in transgenic mice expressing slow skeletal troponin I in the heart J. Physiol. 517 1999 143 157
14. J.C. Kentish, D.T. McCloskey, J. Layland, S. Palmer, J.M. Leiden, and A.F. Martin Phosphorylation of troponin-I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle Circ. Res. 88 2001 1059 1065
15. T.J. Herron, S. Korte, and K.S. Mcdonald Power output is increased after phosphorylation of myofibrillar proteins in rat skinned cardiac myocytes Circ. Res. 89 2001 1184 1190
16. P.P. de Tombe, and H.E.D.J. ter Keurs Lack of effect of isoproterenol on unloaded velocity of sarcomere shortening in rat cardiac trabeculae Circ. Res. 68 1991 382 391
17. P.A. Hofmann, and J.H.I. Lange Effects of phosphorylation of Troponin I and C-protein on isometric tension and velocity of unloaded shortening in skinned single cardiac myocytes from rats Circ. Res. 74 1994 718 726
18. P.M.L. Janssen, and P.P. de Tombe Protein kinase A does not alter unloaded velocity of sarcomere shortening in skinned rat cardiac trabeculae Am. J. Physiol. 42 1997 H2415 H2422
19. E.C. Johns, S.J. Simnett, I.P. Mulligan, and C.C. Ashley Troponin I phosphorylation does not increase the rate of relaxation following laser flash photolysis of diazo-2 in guinea-pig skinned trabeculae Pflügers Arch. 433 1997 842 844
20. B.M. Wolska, G.M. Arteaga, J.R. Pena, G. Nowak, R.M. Phillips, and S. Sahai Expression of slow skeletal troponin I in hearts of phospholamban knockout mice alters the relaxant effect of β-adrenergic stimulation Circ. Res. 90 2002 882 888
21. J.R. Pena, and B.M. Wolska Troponin I phosphorylation plays an important role in the relaxant effect of β-adrenergic stimulation in mouse hearts Cardiovasc. Res. 61 2004 756 763
22. J. Layland, D.J. Grieve, A.C. Cave, E. Sparks, R.J. Solaro, and A.M. Shah Essential role of troponin I in the positive inotropic response to isoprenaline in mouse hearts contracting auxotonically J. Physiol. 556 2004 835 847
23. Y. Pi, K.R. Kemnitz, D. Zhang, E.G. Kranias, and J.W. Walker Phosphorylation of troponin I controls cardiac twitch dynamics. Evidence from phosphorylation site mutants expressed on a troponin-I null background Circ. Res. 90 2002 649 656
24. 2+ sensitivity and ATPase activity in the mouse myocardium J. Physiol. 552 2003 845 857
25. E. Takimoto, D.G. Soergel, P.M.L. Janssen, L.B. Stull, D.A. Kass, and A.M. Murphy Frequency- and afterload-dependent cardiac modulation in vivo by troponin I with constitutively active protein kinase A phosphorylation sites Circ. Res. 94 2004 496 504
26. C.W. Tong, R.D. Gaffin, D.C. Zawieja, and M. Muthuchamy Roles of phosphorylation of myosin binding protein-C and troponin I in mouse cardiac muscle twitch dynamics J. Physiol. 558 2004 927 941
27. L. Li, J. DeSantiago, G.X. Chu, E.G. Kranias, and D.M. Bers Phosphorylation of phospholamban and troponin I in β-adrenergic-induced acceleration of cardiac relaxation Am. J. Physiol. 278 2000 H769 H779
28. J. Layland, and J.C. Kentish Myofilament-based relaxant effect of isoprenaline revealed during work-loop contractions in rat cardiac trabeculae J. Physiol. 544 2002 171 182
29. W. Luo, I.L. Grupp, J. Harrer, S. Ponniah, G. Grupp, and J.J. Duffy Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of β-agonist stimulation Circ. Res. 75 1994 401 409
30. 2+ Am. J. Physiol. 271 1996 C391 C397
31. Y. Takeishi, G.X. Chu, D.M. Kirkpatrick, Z. Li, H. Wakasaki, and E.G. Kranias In vivo phosphorylation of cardiac troponin I by protein kinase C beta 2 decreases cardiomyocyte calcium responsiveness and contractility in transgenic mouse hearts J. Clin. Invest. 102 1998 72 78
32. D.E. Montgomery, B.M. Wolska, W.G. Pyle, B.B. Roman, J.C. Dowell, and P.M. Buttrick α-Adrenergic response and myofilament activity in mouse hearts lacking PKC phosphorylation sites on cardiac TnI Am. J. Physiol. 282 2002 H2397 H2405
33. Y.Q. Pi, R. Sreekumar, X.P. Huang, and J.W. Walker Positive inotropy mediated by diacylglycerol in rat ventricular myocytes Circ. Res. 81 1997 92 100
34. M.V. Westfall, and A.R. Bortonn Role of troponin I phosphorylation in protein kinase C-mediated enhanced contractile performance of rat myocytes J. Biol. Chem. 278 2003 33694 33700
35. 2+-sensitive isoforms in the failing human heart Circulation 99 1999 384 391
36. B.B. Roman, P.H. Goldspink, E. Spaite, D. Urboniene, R. McKinney, and D.L. Geenen Inhibition of PKC phosphorylation of cTnI improves cardiac performance in vivo Am. J. Physiol. 286 2004 H2089 H2095
37. E.M. Burkart, M.P. Sumandea, T. Kobayashi, M. Nili, A.F. Martin, and E. Homsher Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity J. Biol. Chem. 28 2003 11265 11272
38. T.A. Noland, R.L. Raynor, and J.F. Kuo 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. 264 1989 20778 20785
39. W.G. Pyle, M.P. Sumandea, R.J. Solaro, and P.P. de Tombe Troponin I serines 43/45 and regulation of cardiac myofilament function Am. J. Physiol. 283 2002 H1215 H1224
40. G.A. MacGowan, C. Evans, T.C.-C. Hu, D. Debrah, S. Mullet, and H.H. Chen Troponin I protein kinase C phosphorylation sites and ventricular function Cardiovasc. Res. 63 2004 245 255
41. 2+-stimulated MgATPase of reconstituted actomyosin S-1 J. Biol. Chem. 270 1995 25445 25454
42. G.A. MacGowan, C. Du, D.B. Cowan, C. Stamm, F.X. McGowan, and R.J. Solaro Ischemic dysfunction in transgenic mice overexpressing troponin I lacking protein kinase C phosphorylation sites Am. J. Physiol. 280 2001 H835 H843
43. G. McClellan, A. Weisberg, and S. Winegrad Effect of endothelin-1 on actomyosin ATPase activity. Implications for the efficiency of contraction Circ. Res. 78 1996 1044 1050
44. K. Yuasa, H. Michibata, and N. Yanaka A novel interaction of cGMP-dependent protein kinase I with troponin T J. Biol. Chem. 274 1999 37429 37434
45. K.C. Wollert, S. Yurukova, A. Kilic, F. Begrow, B. Fiedler, and S. Gambaryan Increased effects of C-type natriuretic peptide on contractility and calcium regulation in murine hearts overexpressing cyclic GMP-dependent protein kinase I Br. J. Pharmacol. 140 2003 1227 1236
46. D.K. Blumenthal, J.T. Stull, and G.N. Gill Phosphorylation of cardiac troponin by guanosine 3′:5′-monophosphate-dependent protein kinase J. Biol. Chem. 253 1978 334 336
47. A.M. Shah Paracrine modulation of heart cell function by endothelial cells Cardiovasc. Res. 31 1996 847 867
48. J.-M. Brusq, E. Mayoux, L. Guigui, and J. Kirilovsky Effect of C-type natriuretic peptide on rat cardiac contractility Br. J. Pharmacol. 128 1999 206 212
49. M. Pierkes, S. Gambaryan, P. Boknik, S.M. Lohmann, W. Schmitz, and R. Potthast Increased effects of C-type natriuretic peptide on cardiac ventricular contractility and relaxation in guanylyl cyclase A-deficient mice Cardiovasc. Res. 53 2002 852 861
50. F. Brunner, and G. Wölkart Peroxynitrite-induced cardiac depression: role of myofilament desensitization and cGMP pathway Cardiovasc. Res. 60 2003 355 364
51. G. Pfitzer, J.C. Ruegg, V. Flockerzi, and F. Hofmann cGMP-dependent protein kinase decreases calcium sensitivity of skinned cardiac fibres FEBS Lett. 149 1982 171 175
52. R.J. Hajjar, R.H.G. Schwinger, U. Schmidt, C.S. Kim, D. Lebeche, and A.A. Doye Myofilament calcium regulation in human myocardium Circulation 101 2000 1679 1685
53. D.L. Brutsaert, A.L. Meulemans, K.R. Sipido, and S. Sys Effects of damaging the endocardial surface on the mechanical performance of isolated cardiac muscle Circ. Res. 62 1988 358 366
54. W.J. Paulus, P.J. Vantrimpont, and A.M. Shah Acute effects of nitric oxide on left ventricular relaxation and diastolic distensibility in humans Circulation 89 1994 2070 2078
55. 2+ in intact cardiac myocytes Circ. Res. 74 1994 970 978
56. M.G. Vila-Petroff, A. Younes, J. Egan, E.G. Lakatta, and S.J. Sollott Activation of distinct cAMP-dependent and cGMP-dependent pathways by nitric oxide in cardiac myocytes Circ. Res. 84 1999 1020 1031
57. J. Layland, J.-M. Li, and A.M. Shah Role of cyclic GMP-dependent protein kinase in the contractile response to exogenous nitric oxide in rat cardiac myocytes J. Physiol. 540 2002 457 467
58. 2+-independent manner in cardiac myocytes: role of troponin I phosphorylation Biochem. Biophys. Res. Commun. 256 1999 398 403
59. J.W. Wegener, H. Nawrath, W. Wolfsgruber, S. Kuhbandner, C. Werner, and F. Hofmann cGMP-dependent protein kinase I mediates the negative inotropic effect of cGMP in the murine myocardium Circ. Res. 90 2002 18 20
60. N. Ito, J. Bartunek, K.W. Spitzer, and B.H. Lorell Effects of the nitric oxide donor sodium nitroprusside on intracellular pH and contraction in hypertrophied myocytes Circulation 95 1997 2303 2311
61. 21-activated kinase-1 (Pak1) in cardiac myocytes Circ. Res. 94 2004 194 200
62. Q. Liu, and P.A. Hofmann Antiadrenergic effects of adenosine A1 receptor-mediated protein phosphatase 2a activation in the heart Am. J. Physiol. 283 2002 H1314 H1321
63. K.T. Strang, R.M. Mentzer, and R.L. Moss Slowing of shortening velocity of rat cardiac myocytes by adenosine receptor stimulation regardless of β-adrenergic stimulation J. Physiol. 486 1995 679 688
64. Q. Liu, and P.A. Hofmann Modulation of protein phosphatase 2a by adenosine A1 receptors in cardiomyocytes: role for p38 MAPK Am. J. Physiol. 285 2003 H97 H103
65. P. Liao, S.Q. Wang, S. Wang, M. Zheng, M. Zheng, and S.J. Zhang p38 Mitogen-activated protein kinase mediates a negative inotropic effect in cardiac myocytes Circ. Res. 90 2002 190 196
66. Y. Chen, R. Rajashree, Q. Liu, and P.A. Hofmann Acute p38 MAPK activation decreases force development in ventricular myocytes Am. J. Physiol. 285 2003 H2578 H2586
67. N. Buscemi, D.B. Foster, I. Neverova, and J.E. van Eyk 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. 91 2002 509 516
68. G. Hasenfuss, and B. Pieske Calcium cycling in congestive heart failure J. Mol. Cell. Cardiol. 34 2002 951 969
69. E.D. Pagani, A.A. Alousi, A.M. Grant, T.M. Older, S.W. Dziuban, and P.D. Allen Changes in myofibrillar content and Mg-ATPase activity in ventricular tissue from patients with heart failure caused by coronary artery disease, cardiomyopathy or mitral valve insufficiency Circ. Res. 63 1988 380 385
70. M.R. Wolff, S.H. Buck, S.W. Stoker, M.L. Greaser, and R.M. Mentzer Myofibrillar calcium sensitivity of isometric tension is increased in human dilated cardiomyopathies. Role of altered β-adrenergically mediated protein phosphorylation J. Clin. Invest. 98 1996 167 176
71. R.J. Hajjar, and J.K. Gwathmey Cross-bridge dynamics in human ventricular myocardium. Regulation of contractility in the failing heart Circulation 86 1992 1819 1826
72. T. Ruf, H. Schultebaukloh, J. Ludemann, H. Posival, F. Beyersdorf, and H. Just Alterations of cross-bridge kinetics in human atrial and ventricular myocardium Cardiovasc. Res. 40 1998 580 590
73. 2+ sensitivity J. Mol. Cell. Cardiol. 34 2002 469 482
74. G. Hasenfuss, L.A. Mulieri, E.M. Blanchard, C. Holubarsch, B.J. Leavitt, and F. Ittleman Energetics of isometric force development in control and volume-overloaded human myocardium. Comparison with animal species Circ. Res. 68 1991 836 846
75. T. Noguchi, Y. Kihara, K.J. Begin, J.A. Gorga, K.A. Palmiter, and M.M. LeWinter Altered myocardial thin-filament function in the failing Dahl salt-sensitive rat heart. Amelioration by endothelin blockade Circulation 107 2003 630 635
76. A. El-Armouche, T. Pamminger, D. Ditz, O. Zolk, and T. Eschenhagen Decreased protein and phosphorylation level of the protein phosphatase inhibitor-1 in failing human hearts Cardiovasc. Res. 61 2004 87 93
77. J. Neumann, T. Eschenhagen, L.R. Jones, B. Linck, W. Schmitz, and H. Scholz Increased expression of cardiac phosphatases in patients with end-stage heart failure J. Mol. Cell. Cardiol. 29 1997 265 272
78. B.K. McConnell, C.S. Moravec, and M. Bond Troponin-I phosphorylation and myofilament calcium sensitivity during decompensated cardiac hypertrophy Am. J. Physiol. 274 1998 H385 H396
79. 2 isoform in myocardium causes cardiomyopathy Proc. Natl. Acad. Sci. U. S. A. 94 1997 9320 9325
80. J.C. Bowman, S.F. Steinberg, T. Jiang, D.L. Geenen, G.I. Fishman, and P.M. Buttrick Expression of protein kinase Cβ in the heart causes hypertrophy in adult mice and sudden death in neonates J. Clin. Invest. 100 1997 2189 2195
81. 2+ transients of mouse heart myocytes conditionally expressing PKCβ Am. J. Physiol. 280 2001 C1114 C1120
82. P.H. Goldspink, D.E. Montgomery, L.A. Walker, D. Urboniene, R.D. McKinney, and D.L. Geenen Protein kinase Cε overexpression alters myofilament properties and composition during the progression of heart failure Circ. Res. 95 2004 424 432
83. R.M. Grocott-Mason, and A.M. Shah Cardiac dysfunction in sepsis: new theories and clinical implications Intensive Care Med. 24 1998 286 295
84. F.M. Powers, S. Farias, H. Minami, A.F. Martin, R.J. Solaro, and W.R. Law Cardiac myofilament protein function is altered during sepsis J. Mol. Cell. Cardiol. 30 1998 967 978
85. F.H. Khadour, D. Panas, P. Ferdinandy, C. Schulze, T. Csont, and M.M. Lalu Enhanced NO and superoxide generation in dysfunctional hearts from endotoxemic rats Am. J. Physiol. 283 2002 H1108 H1115
86. B. Tavernier, D. Garrigue, C. Boulle, B. Vallet, and P. Adnet Myofilament calcium sensitivity is decreased in skinned cardiac fibres of endotoxin-treated rabbits Cardiovasc. Res. 38 1998 472 479
87. 2+ responsiveness Am. J. Physiol. 274 1998 H580 H590
88. B. Tavernier, J.-M. Li, M.M. El-Omar, S. Lanone, Z.K. Yang, and I.P. Trayer Cardiac contractile impairment associated with increased phosphorylation of troponin I in endotoxaemic rats FASEB J. 2000 10.1096/fj.00-0433fje
89. 2+ in cardiac myocytes Circ. Res. 81 1997 1011 1020
90. 2+ sensitivity but normal mitochondrial function in septic heart Am. J. Crit. Care Med. 163 2000 362 367
91. L.-L. Wu, C. Tang, and M.-S. Liu Altered phosphorylation and calcium sensitivity of cardiac myofibrillar proteins during sepsis Am. J. Physiol. 281 2001 R408 R416
92. J. Layland, A.C. Cave, D.J. Grieve, E. Sparks, R.J. Solaro, and A.M. Shah Expression of slow skeletal troponin I protects against endotoxaemia induced contractile dysfunction in mouse cardiac myocytes Heart 90 2004 A24 [Abstract]