N-terminal phosphorylation of cardiac troponin-I reduces length-dependent calcium sensitivity of contraction in cardiac muscle

Journal of Physiology

Volumn 591, Issue 2, 2013, Pages 475-490

  Rao, Vijay S ^a   Korte, F Steven ^a   Razumova, Maria V ^a   Feest, Erik R ^a   Hsu, Hsiaoman ^b   Irving, Thomas C ^b   Regnier, Michael ^a   Martyn, Donald A ^a  

^a University of Washington   (United States)

^b ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CARDIAC TROPONIN I; CONNECTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; MYOSIN BINDING PROTEIN C; TROPONIN I; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CONTROLLED STUDY; HEART CONTRACTION; HEART MUSCLE CONTRACTILE FORCE; HEART OUTPUT; MALE; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SARCOMERE LENGTH; SENSITIVITY ANALYSIS; THIN FILAMENT;

ANIMALS; CALCIUM; CARRIER PROTEINS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HEART; MALE; MUSCLE PROTEINS; MUTATION; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOFIBRILS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; TROPONIN I;

EID: 84872386336     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.241604     Document Type: Article

References (72)

1. Adhikari BB, Regnier M, Rivera AJ, Kreutziger KL & Martyn DA (2004). Cardiac length dependence of force and force redevelopment kinetics with altered crossbridge cycling. Biophys J 87, 1784-1794.
2. Arteaga GM, Palmiter KA, Leiden JM & Solaro RJ (2000). Attenuation of length dependence of calcium activation in myofilaments of transgenic mouse hearts expressing slow skeletal troponin I. J Physiol 526, 541-549.
3. 2+ sensitivity and cross-bridge cycling. J Biol Chem 285, 5674-5682.
4. Bers DM (2002). Cardiac excitation-contraction coupling. Nature 415, 198-205.
5. Burkart EM, Sumandea MP, Kobayashi T, Nili M, Martin AF, Homsher E & Solaro RJ (2003). Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J Biol Chem 278, 11 265-11 272.
6. Cazorla O, Szilagyi S, Vignier N, Salazar G, Kramer E, Vassort G, Carrier L & Lacampagne A (2006). Length and protein kinase A modulations of myocytes in cardiac mysoin binding protein C-deficient mice. Cardiovasc Res 69, 370-380.
7. Cazorla O, Wu Y, Irving TC & Granzier H (2001). Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ Res 88, 1028-1035.
8. Chandra M, Dong WJ, Pan BS, Cheung HC & Solaro RJ (1997). Effects of protein kinase A phosphorylation on signaling between cardiac troponin I and the N-terminal domain of cardiac troponin C. Biochem 36, 13, 305-13, 311.
9. 2+ as a result of phosphorylation of cardiac myosin-binding protein C. J Gen Physiol 186, 615-627.
10. Colson BA, Bekyarova T, Fitzsimons DP, Irving TC & Moss RL (2007). Radial displacement of myosin-crossbridges in mouse myocardium due to ablation of myosin binding protein C. J Mol Biol 376, 36-41.
11. Colson BA, Bekyarova T, Locher MR, Fitzsimmons DP, Irving TC & Moss RL (2008). Protein kinase A-mediated phosphorylation of cMyBP-C increases proximity of myosin heads to actin in resting myocardium. Circ Res 103, 244-251.
12. Colson BA, Locher MR, Bekyarova T, Patel JR, Fitzsimons DP, Irving TC & Moss RL (2010). Differential roles of regulatory light chain and myosin binding protein-C phosphorylation in the modulation of cardiac force development. J Physiol 588, 981-993.
13. Dohet C, Al-Hillawi E, Trayer IP & Ruegg JC (1995). Reconstitution of skinned cardiac fibres with human recombinant cardiac troponin-I mutants and troponin-C. FEBS Lett 377, 131-134.
14. Dong W-J, Jayasundar JJ, An J, Xing J & Cheung HC (2007). Effects of PKA phosphorylation of cardiac troponin I and strong crossbridge on conformational transitions of the N-domain of cardiac troponin C in regulated thin filaments. Biochemistry 46, 9752-9761.
15. Fabiato A (1988). Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol 157, 378-417.
16. Farman GP, Gore D, Allen E, Schoenfelt K, Irving TC & de Tombe PP (2011). Myosin head orientation: a structural determinant for the Frank-Starling relationship. Am J Physiol Heart Circ Physiol 300, H2155-H2160.
17. Finley N, Abbott MB, Abusamhadneh E, Gaponenko V, Dong W, Gasmi-Seabrook G, Howarth JW, Rance M, Solaro RJ, Cheung HC & Rosevear PR (1999). NMR analysis of cardiac troponin C-troponin I complexes: effects of phosphorylation. FEBS Lett 453, 107-112.
18. Fischetti R, Stepanov S, Rosenbaum G, Barrea R, Black E, Gore D, Heurich R, Kondrashkina E, Kropf AJ, Wang S, Zhang K, Irving TC & Bunker GB (2004). The BioCAT undulator beamline 18ID: a facility for biological non-crystalline diffraction and X-ray absorption spectroscopy at the Advanced Photon Source. J Synchrotron Radiat 11, 399-405.
19. Flashman E, Redwood C, Moolman-Smook J & Watkins H (2004). Cardiac myosin binding protein C: its role in physiology and disease. Circ Res 94, 1279-1289.
20. Fuchs F & Martyn DA (2005). Length-dependent activation in cardiac muscle: some remaining questions. J Musc Res Cell Motil 26, 199-212.
21. Fukuda N, Wu Y, Nair P & Granzier H (2005). Phosphorylation of titin modulates passive stiffness of cardiac muscle in a titin isoform-dependent manner. J Gen Physiol 125, 257-271.
22. Gaponenko V, Abusamhadneh E, Abbott MB, Finley N, Gasmi-Seabrook G, Solaro RJ, Rance M & Rosevear PR (1999). Effects of troponin I phosphorylation on conformational exchange in the regulatory domain of cardiac troponin C. J Biol Chem 274, 16, 681-16, 684.
23. Gillis TE, Martyn DA, Rivera AJ & Regnier M (2007). Investigation of thin filament near-neighbour regulatory unit interactions during force development in skinned cardiac and skeletal muscle. J Physiol 580, 561-576.
24. Gordon AM, Homsher E & Regnier M (2000). Regulation of contraction in striated muscle. Physiol Rev 80, 853-924.
25. Granzier H, Labeit D, Wu Y & Labeit S (2002). Titin as a modular spring: emerging mechanisms for elasticity control by titin in cardiac physiology and pathophysiology. J Musc Res Cell Motil 23, 457-471.
26. Granzier H & Labeit S (2002). Cardiac titin: an adjustable multi-functional spring. J Physiol 541, 335-342.
27. Granzier H & Labeit S (2004). The giant protein Titin: a major player in myocardial mechanics, signalling and disease. Circ Res 94, 284-295.
28. Hanft LM & McDonald KS (2009). Sarcomere length dependence of power output is increased after PKA treatment in rat cardiac myocytes. Am J Physiol Heart Circ Physiol 296, H1524-H1531.
29. Harris SP, Rostkova EV, Gautel M & Moss RL (2004). Binding of myosin binding protein-C to myosin subfragment S2 affects contractility independent of a tether mechanism. Circ Res 95, 930-936.
30. Howarth J, Meller J, Solaro RJ, Trewhella J & Rosevear PR (2007). Phosphorylation-dependent conformational transition of the cardiac specific N-extension of troponin-I in cardiac troponin. J Mol Biol 373, 706-722.
31. Irving TC, Konhilas J, Perry D, Fischetti R & de Tombe PP (2000). Myofilament lattice spacing as a function of sarcomere length in isolated rat myocardium. Am J Physiol Heart Circ Physiol 279, H2568-H2573.
32. Irving TC & Millman BM (1989). Changes in thick filament structure during compression of the filament lattice in relaxed frog sartorius muscle. J Muscle Res Cell Motil 10, 385-394.
33. Kajiwara H, Morimoto S, Fukuda N, Ohtsuki I & Kurihara S (2000). Effects of troponin I phosphorylation by protein kinase A on length-dependence of tension in rat skinned myocardium. Biochem Biophys Res Comm 272, 104-110.
34. Kensler RW, Shaffer JF & Harris SP (2011). Binding of N-terminal fragment C0-C2 of cardiac MyBP-C to cardiac F-actin. J Struct Biol 174, 44-51.
35. Kentish JC, McCloskey DT, Layland J, Palmer S, Leiden JM, Martin AF & Solaro RJ (2001). Phosphorylation of troponin I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle. Circ Res 88, 1059-1065.
36. Kobayashi T & Solaro RJ (2005). Calcium, thin filaments and the integrative biology of cardiac contractility. Annu Rev Physiol 67, 39-67.
37. Kohler J, Chen Y, Brenner B, Gordon AM, Kraft T, Martyn DA, Regnier M, Rivera AJ, Wang CK & Chase PB (2003). Familial hypertrophic cardiomyopathy mutations in troponin I (K183D, G203S, K206Q) enhance filament sliding. Physiol Genomics 14, 117-128.
38. Konhilas J, Irving TC, Wolska B, Jweied EE, Martin A, Solaro RJ & de Tombe PP (2003). Troponin I in the murine myocardium: influence on length dependent activation and interfilament spacing. J Physiol 547, 951-961.
39. Konhilas JP, Wolska BM, Martin AF, Solaro RJ & de Tombe PP (2000). PKA modulates length-dependent activation in murine myocardium. Biophys J 78, 108A.
40. Kruger M & Linke WA (2006). Protein kinase-A phosphorylates titin in human heart muscle and reduces myofibrillar passive tension. J Muscle Res Cell Motil 27, 435-444.
41. Kulikovskaya I, McClellan G, Flavigny J, Carrier L & Winegrad S (2003). Effect of MyBP-C binding to actin on contractility in heart muscle. J Gen Physiol 122, 761-774.
42. Layland J, Solaro RJ & Shah AM (2005). Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc Res 66, 12-21.
43. Li MX, Wang X, Lindhout DA, Buscemi N, van Eyk J & Sykes BD (2003). Phosphorylation and mutation of cardiac troponin I deferentially destabilize the interaction of the functional regions of troponin I with troponin C. Biochemistry 42, 14 460-14 468.
44. Li MX, Wang X & Sykes BD (2004). Structure based insights into the role of troponin in cardiac muscle pathophysiology. J Musc Res Cell Motil 25, 559-579.
45. Martyn DA, Adhikari BB, Regnier M, Gu J, Xu S & Yu L (2004). Response of equatorial x-ray reflections and stiffness to altered sarcomere length and myofilament lattice spacing in relaxed skinned cardiac muscle. Biophys J 86, 1002-1011.
46. Martyn DA & Smith L (2005). The temperature dependence of length-dependent activation in cardiac muscle. Biophys J 88, 120a.
47. Millman B (1998). The filament lattice of striated muscle. Physiol Rev 78, 360-391.
48. Moir AJG, Solaro RJ & Perry SV (1980). The site of phosphorylation of troponin I in the perfused rabbit heart. Biochem J 185, 505-513.
49. Moolman-Smook J, Flashman E, de Lange W, Li Z, Corfield V, Redwood C & Watkins H (2002). Identification of novel interactions between domains of myosin binding protein-C that are modulated by hypertrophic missense mutations. Circ Res 91, 704-711.
50. 2+-stimulated MgATPase of reconstituted actomyosin S-1. J Biol Chem 270, 25, 445-25, 454.
51. 2+-sensitivity of force and activation dependence of the kinetics of myocardial force development. Am J Physiol Heart Circ Physiol 287, H2712-H2718.
52. Potter JD (1982). Preparation of troponin and its subunits. Methods Enzymol 85, 241-263.
53. Regnier M, Martin H, Barsotti RJ, Martyn DA & Clemmens EW (2004). Cross-bridge versus thin filament contributions to the level and rate of force development in cardiac muscle. Biophys J 87, 1815-1824.
54. 2+-regulatory site of bovine cardiac troponin. J Biol Chem 257, 260-263.
55. 2+ and myosin-induced activation of heart muscle. J Mol Biol 340, 295-305.
56. Sadayappan S, Finley N, Howarth J, Osinka H, Klevitsky R, Lorenz JN, Rosevear PR & Robbins J (2008). Role of the acidic N¢ region of cardiac troponin I in regulating myocardial function. FASEB J 22, 1246-1257.
57. Shaffer JF, Kensler RW & Harris SP (2009). The myosin-binding Protein C motif binds to f-actin in a phosphorylation sensitive manner. J Biol Chem 284, 12, 318-12, 327.
58. 2+ activation in skinned cardiac muscle. J Mol Cell Cardiol 31, 2115-2125.
59. Stelzer JE, Larsson L, Fitzsimmons DP & Moss RL (2006). Activation dependence of stretch activation in mouse skinned myocardium: implications for ventricular function. J Gen Physiol 127, 95-107.
60. Sumandea MP, Burkart EM, Kobayashi T, de Tombe PP & Solaro RJ (2004). Molecular and integrated biology of thin filament protein phosphorylation in heart muscle. Ann NY Acad Sci 1015, 39-52.
61. Tachampa K, Kobayashi T, Wang H, Martin AF, Biesiadecki BJ, Solaro RJ & de Tombe PP (2008). Increased cross-bridge cycling kinetics after exchange of C-terminal truncated troponin I in skinned rat cardiac muscle. J Biol Chem 283, 15 114-15 121.
62. Tachampa K, Wang H, Farman GP & de Tombe PP (2007). Cardiac troponin I threonine 144: role in myofilament length dependent activation. Circ Res 101, 1081-1083.
63. Tong CW, Stelzer JE, Greaser ML, Powers PA & Moss RL (2008). Acceleration of crossbridge kinetics by protein kinase A phosphorylation of cardiac myosin binding protein C modulates cardiac function. Circ Res 103, 974-982.
64. Verduyn SC, Zaremba R, van der Velden J & Steinen GJM (2007). Effects of contractile protein phosphorylation on force development in permeabilized rat cardiac myocytes. Basic Res Cardiol 102, 476-487.
65. Wattanapermpool J, Guo X & Solaro RJ (1995). The unique amino-terminal peptide of cardiac troponin I regulates myofibrillar activity only when it is phosphorylated. J Mol Cell Cardiol 27, 1383-1391.
66. Whitten AE, Jeffries CM, Harris SP & Trewhella J (2008). Cardiac myosin-binding protein C decorates F-actin: implications for cardiac function. Proc Natl Acad Sci USA 105, 18 360-18 365.
67. Winegrad S (2000). Myosin binding protein C, a potential regulator of cardiac contractility. Circ Res 86, 6-7.
68. Wojdyr M (2010). Fityk: a general-purpose peak fitting program. J Appl Crystallogr 43, 1126-1128.
69. Xing J, Chinnaraj M, Zhang Z, Cheung HC & Dong W-J (2008). Structural studies of interactions between cardiac troponin I and actin in regulated thin filament using Forster Resonance Energy Transfer. Biochemistry 47, 13 383-13 393.
70. Yamasaki R, Wu Y, McNabb M, Greaser M, Labeit S & Granzier H (2002). Protein kinase A phosphorylates titin's cardiac-specific N2B domain and reduces passive tension in rat cardiac myocytes. Circ Res 90, 1181-1188.
71. Zhang R, Zhao J, Mandveno A & Potter JD (1995a). Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation. Circ Res 76, 1028-1035.
72. 2+ affinity of cardiac troponin C. J Biol Chem 270, 30, 773-30, 780.