Tri-modal regulation of cardiac muscle relaxation; intracellular calcium decline, thin filament deactivation, and cross-bridge cycling kinetics

Biophysical Reviews

Volumn 6, Issue 3-4, 2014, Pages 273-289

  Biesiadecki, Brandon J ^a   Davis, Jonathan P ^a   Ziolo, Mark T ^a   Janssen, Paul M L ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Calcium handling; Cardiac relaxation; Contraction; Diastole; Kinetics; Myofilaments

Indexed keywords

ADENOSINE DIPHOSPHATE; CALCIUM CHANNEL L TYPE; NEURONAL NITRIC OXIDE SYNTHASE; PEROXYNITRITE; PROTEIN KINASE C; TROPONIN;

ADRENERGIC STIMULATION; BODY EQUILIBRIUM; CALCIUM CELL LEVEL; DETERIORATION; DISSOCIATION; GENE CONTROL; HEART MUSCLE RELAXATION; HEART OUTPUT; HEART RATE; HEART RATE VARIABILITY; HUMAN; KINETICS; LIGHT CHAIN; NONHUMAN; OXYGEN CONSUMPTION; PHOSPHORYLATION; PROTEIN EXPRESSION; REVIEW; SARCOPLASMIC RETICULUM; SODIUM CALCIUM EXCHANGE; THIN FILAMENT;

EID: 84908351058     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-014-0143-5     Document Type: Review

References (164)

1. Adhikari BB, Regnier M, Rivera AJ, Kreutziger KL, Martyn DA (2004) Cardiac length dependence of force and force redevelopment kinetics with altered cross-bridge cycling. Biophys J 87(3):1784–1794
2. Allen DG, Kentish JC (1985) The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol 17(9):821–840
3. Allen DG, Kurihara S (1979) Calcium transients at different muscle lengths in rat ventricular muscle [proceedings]. J Physiol Lond 292:68P–69P
4. Allen DG, Kurihara S (1982) The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol Lond 327:79–94
5. Alvarez BV, Perez NG, Ennis IL, Camilion de Hurtado MC, Cingolani HE (1999) Mechanisms underlying the increase in force and Ca(2+) transient that follow stretch of cardiac muscle: a possible explanation of the Anrep effect. Circ Res 85(8):716–722
6. Anderson BR, Granzier HL (2012) Titin-based tension in the cardiac sarcomere: molecular origin and physiological adaptations. Prog Biophys Mol Biol 110(2–3):204–217
7. Ayaz-Guner S, Zhang J, Li L, Walker JW, Ge Y (2009) In vivo phosphorylation site mapping in mouse cardiac troponin I by high resolution top-down electron capture dissociation mass spectrometry: Ser22/23 are the only sites basally phosphorylated. Biochemistry 48(34):8161–8170
8. Barany M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50((6):Suppl):197–218
9. Barefield D, Sadayappan S (2010) Phosphorylation and function of cardiac myosin binding protein-C in health and disease. J Mol Cell Cardiol 48(5):866–875
10. Bassani RA, Bassani JW, Bers DM (1995) Relaxation in ferret ventricular myocytes: role of the sarcolemmal Ca ATPase. Pflugers Arch 430(4):573–578
11. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, Nadal-Ginard B, Silvestri F, Leri A, Beltrami CA, Anversa P (2001) Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 344(23):1750–1757
12. Bencsik P, Kupai K, Giricz Z, Gorbe A, Huliak I, Furst S, Dux L, Csont T, Jancso G, Ferdinandy P (2008) Cardiac capsaicin-sensitive sensory nerves regulate myocardial relaxation via S-nitrosylation of SERCA: role of peroxynitrite. Br J Pharmacol 153(3):488–496
13. Bers DM (2001) Excitation-Contraction Coupling and Cardiac Contractile Force. Kluwer, Dordrecht
14. Bers DM (2002a) Cardiac excitation-contraction coupling. Nature 415(6868):198–205
15. Bers DM (2002b) Cardiac Na/Ca Exchange Function in Rabbit, Mouse and Man: What’s the Difference? J Mol Cell Cardiol 34(4):369–373
16. Bers DM, Berlin JR (1995) Kinetics of [Ca]i decline in cardiac myocytes depend on peak [Ca]i. Am J Physiol 268(1 Pt 1):C271–277
17. Bers DM, Ziolo MT (2001) When is cAMP not cAMP? Effects of compartmentalization. Circ Res 89(5):373–375
18. Biesiadecki BJ, Kobayashi T, Walker JS, John Solaro R, de Tombe PP (2007a) The troponin C G159D mutation blunts myofilament desensitization induced by troponin I Ser23/24 phosphorylation. Circ Res 100(10):1486–1493
19. Biesiadecki BJ, Kobayashi T, Walker JS, Solaro RJ, de Tombe PP (2007b) The troponin C G159D mutation blunts myofilament desensitization induced by troponin I Ser23/24 phosphorylation. Circ Res 100(10):1486–1493
20. Bilchick KC, Duncan JG, Ravi R, Takimoto E, Champion HC, Gao WD, Stull LB, Kass DA, Murphy AM (2007) Heart failure-associated alterations in troponin I phosphorylation impair ventricular relaxation-afterload and force-frequency responses and systolic function. Am J Physiol Heart Circ Physiol 292(1):H318–325
21. Boontje NM, Merkus D, Zaremba R, Versteilen A, de Waard MC, Mearini G, de Beer VJ, Carrier L, Walker LA, Niessen HW, Dobrev D, Stienen GJ, Duncker DJ, van der Velden J (2011) Enhanced myofilament responsiveness upon beta-adrenergic stimulation in post-infarct remodeled myocardium. J Mol Cell Cardiol 50(3):487–499
22. Borlaug BA, Kass DA (2008) Ventricular-vascular interaction in heart failure. Heart Fail Clin 4(1):23–36
23. Bouchard RA, Bose D (1989) Analysis of the interval-force relationship in rat and canine ventricular myocardium. Am J Physiol 257(6 Pt 2):H2036–2047
24. Brutsaert DL, de Clerck NM, Goethals MA, Housmans PR (1978) Relaxation of ventricular cardiac muscle. J Physiol Lond 283(17):469–480
25. Buscemi N, Foster DB, Neverova I, Van Eyk JE (2002) 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(6):509–516
26. 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 phosphorylations in the modulation of cardiac force development. J Physiol 588(Pt 6):981–993
27. Corino VD, Matteucci M, Mainardi LT (2007) Analysis of heart rate variability to predict patient age in a healthy population. Methods Inf Med 46(2):191–195
28. Counihan PJ, Fei L, Bashir Y, Farrell TG, Haywood GA, McKenna WJ (1993) Assessment of heart rate variability in hypertrophic cardiomyopathy. Association with clinical and prognostic features. Circulation 88(4 Pt 1):1682–1690
29. Davis JP, Tikunova SB (2008) Ca(2+) exchange with troponin C and cardiac muscle dynamics. Cardiovasc Res 77(4):619–626
30. Davis J, Norman C, Kobayashi T, Solaro RJ, Swartz DR, Tikunova SB (2007) Effects of Thin and Thick Filament Proteins on Calcium Binding and Exchange with Cardiac Troponin C. Biophys J 92(9):3195–3206
31. de Tombe PP (1998) Congestive heart failure: role of cross-bridge cycle kinetics [editorial]. Cardiovasc Res 40(3):440–443
32. de Tombe PP, Mateja RD, Tachampa K, Mou YA, Farman GP, Irving TC (2010) Myofilament length dependent activation. J Mol Cell Cardiol 48(5):851–858
33. Deng Y, Schmidtmann A, Redlich A, Westerdorf B, Jaquet K, Thieleczek R (2001) Effects of phosphorylation and mutation R145G on human cardiac troponin I function. Biochemistry 40(48):14593–14602
34. DeSantiago J, Maier LS, Bers DM (2004) Phospholamban is required for CaMKII-dependent recovery of Ca transients and SR Ca reuptake during acidosis in cardiac myocytes. J Mol Cell Cardiol 36(1):67–74
35. Edman KA (1979) The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol Lond 291(7):143–159
36. Ertz-Berger BR, He H, Dowell C, Factor SM, Haim TE, Nunez S, Schwartz SD, Ingwall JS, Tardiff JC (2005) Changes in the chemical and dynamic properties of cardiac troponin T cause discrete cardiomyopathies in transgenic mice. Proc Natl Acad Sci USA 102(50):18219–18224
37. Fitzsimons DP, Patel JR, Moss RL (1998) Role of myosin heavy chain composition in kinetics of force development and relaxation in rat myocardium. J Physiol 513(Pt 1):171–183
38. Foster DB, Noguchi T, VanBuren P, Murphy AM, Van Eyk JE (2003) C-terminal truncation of cardiac troponin I causes divergent effects on ATPase and force: implications for the pathophysiology of myocardial stunning. Circ Res 93(10):917–924
39. Frank O (1895) Zur Dynamik des Herzmuskels. Z Biol 32:370–447
40. Gautel M, Zuffardi O, Freiburg A, Labeit S (1995) Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: a modulator of cardiac contraction? EMBO J 14(9):1952–1960
41. Ginsburg KS, Bers DM (2005) Isoproterenol does not enhance Ca-dependent Na/Ca exchange current in intact rabbit ventricular myocytes. J Mol Cell Cardiol 39(6):972–981
42. Goldhaber JI (1996) Free radicals enhance Na+/Ca2+ exchange in ventricular myocytes. Am J Physiol 271(3 Pt 2):H823–833
43. Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80(2):853–924
44. Granzier HL, Irving TC (1995) Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68(3):1027–1044
45. Granzier H, Wu Y, Siegfried L, LeWinter M (2005) Titin: physiological function and role in cardiomyopathy and failure. Heart Fail Rev 10(3):211–223
46. Hanft LM, Korte FS, McDonald KS (2008) Cardiac function and modulation of sarcomeric function by length. Cardiovasc Res 77(4):627–636
47. Hernandez OM, Jones M, Guzman G, Szczesna-Cordary D (2007) Myosin essential light chain in health and disease. Am J Physiol Heart Circ Physiol 292(4):H1643–1654
48. Herzig JW, Peterson JW, Ruegg JC, Solaro RJ (1981) Vanadate and phosphate ions reduce tension and increase cross-bridge kinetics in chemically skinned heart muscle. Biochim Biophys Acta 672(2):191–196
49. Hidalgo C, Hudson B, Bogomolovas J, Zhu Y, Anderson B, Greaser M, Labeit S, Granzier H (2009) PKC phosphorylation of titin’s PEVK element: a novel and conserved pathway for modulating myocardial stiffness. Circ Res 105 (7):631–638, 17 pp following 638.
50. High CW, Stull JT (1980) Phosphorylation of myosin in perfused rabbit and rat hearts. Am J Physiol 239(6):H756–764
51. Hofmann PA, Fuchs F (1987) Evidence for a force-dependent component of calcium binding to cardiac troponin C. Am J Physiol 253(4 Pt 1):C541–546
52. Houser SR, Piacentino V 3rd, Weisser J (2000) Abnormalities of calcium cycling in the hypertrophied and failing heart. J Mol Cell Cardiol 32(9):1595–1607
53. James J, Robbins J (2011) Signaling and myosin-binding protein C. J Biol Chem 286(12):9913–9919
54. Janssen PML (2010a) 54th Bowditch Lecture: Myocardial contraction-relaxation coupling. Am J Physiol Heart Circ Physiol 299(6):H1741–1749
55. Janssen PML (2010b) Kinetics of Cardiac Muscle Contraction and Relaxation are Linked and Determined by Properties of the Cardiac Sarcomere. Am J Physiol Heart Circ Physiol 299:H1092–1099
56. Janssen PML, Hunter WC (1995) Force, not sarcomere length, correlates with prolongation of isosarcometric contraction. Am J Physiol Heart Circ Physiol 269:H676–685
57. Janssen PML, Periasamy M (2007) Determinants of frequency-dependent contraction and relaxation of mammalian myocardium. J Mol Cell Cardiol 43(5):523–531
58. Janssen PML, Stull LB, Marban E (2002) Myofilament properties comprise the rate-limiting step for cardiac relaxation at body temperature in the rat. Am J Physiol Heart Circ Physiol 282:H499–H507
59. Jideama NM, Noland TA Jr, Raynor RL, Blobe GC, Fabbro D, Kazanietz MG, Blumberg PM, Hannun YA, Kuo JF (1996) Phosphorylation specificities of protein kinase C isozymes for bovine cardiac troponin I and troponin T and sites within these proteins and regulation of myofilament properties. J Biol Chem 271(38):23277–23283
60. Kamm KE, Stull JT (2011) Signaling to myosin regulatory light chain in sarcomeres. J Biol Chem 286(12):9941–9947
61. Kentish JC, ter Keurs HE, Ricciardi L, Bucx JJ, Noble MI (1986) Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle. Influence of calcium concentrations on these relations. Circ Res 58(6):755–768
62. 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(10):1059–1065
63. Kho C, Lee A, Jeong D, Oh JG, Chaanine AH, Kizana E, Park WJ, Hajjar RJ (2011) SUMO1-dependent modulation of SERCA2a in heart failure. Nature 477(7366):601–605
64. Kobayashi T, Solaro RJ (2005) Calcium, thin filaments, and the integrative biology of cardiac contractility. Annu Rev Physiol 67:39–67
65. Kohr MJ, Wang H, Wheeler DG, Velayutham M, Zweier JL, Ziolo MT (2008) Targeting of phospholamban by peroxynitrite decreases {beta}-adrenergic stimulation in cardiomyocytes. Cardiovasc Res 77(2):353–361
66. Kohr MJ, Traynham CJ, Roof SR, Davis JP, Ziolo MT (2010) cAMP-independent activation of protein kinase A by the peroxynitrite generator SIN-1 elicits positive inotropic effects in cardiomyocytes. J Mol Cell Cardiol 48(4):645–648
67. Kooij V, Saes M, Jaquet K, Zaremba R, Foster DB, Murphy AM, Dos Remedios C, van der Velden J, Stienen GJ (2010) Effect of troponin I Ser23/24 phosphorylation on Ca2 + −sensitivity in human myocardium depends on the phosphorylation background. J Mol Cell Cardiol 48(5):954–963
68. Korte FS, McDonald KS (2007) Sarcomere length dependence of rat skinned cardiac myocyte mechanical properties: dependence on myosin heavy chain. J Physiol 581(Pt 2):725–739
69. Kranias EG, Solaro RJ (1982) Phosphorylation of troponin I and phospholamban during catecholamine stimulation of rabbit heart. Nature 298(5870):182–184
70. Kruger M, Linke WA (2011) The giant protein titin: a regulatory node that integrates myocyte signaling pathways. J Biol Chem 286(12):9905–9912
71. Kruger M, Kohl T, Linke WA (2006) Developmental changes in passive stiffness and myofilament Ca2+ sensitivity due to titin and troponin-I isoform switching are not critically triggered by birth. Am J Physiol Heart Circ Physiol 291(2):H496–506
72. Kruger M, Kotter S, Grutzner A, Lang P, Andresen C, Redfield MM, Butt E, dos Remedios CG, Linke WA (2009) Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circ Res 104(1):87–94
73. Kuster GM, Lancel S, Zhang J, Communal C, Trucillo MP, Lim CC, Pfister O, Weinberg EO, Cohen RA, Liao R, Siwik DA, Colucci WS (2010) Redox-mediated reciprocal regulation of SERCA and Na + −Ca2+ exchanger contributes to sarcoplasmic reticulum Ca2+ depletion in cardiac myocytes. Free Radic Biol Med 48(9):1182–1187
74. Kuster DW, Bawazeer AC, Zaremba R, Goebel M, Boontje NM, van der Velden J (2012) Cardiac myosin binding protein C phosphorylation in cardiac disease. J Muscle Res Cell Motil 33(1):43–52
75. Lancel S, Zhang J, Evangelista A, Trucillo MP, Tong X, Siwik DA, Cohen RA, Colucci WS (2009) Nitroxyl activates SERCA in cardiac myocytes via glutathiolation of cysteine 674. Circ Res 104(6):720–723
76. Lancel S, Qin F, Lennon SL, Zhang J, Tong X, Mazzini MJ, Kang YJ, Siwik DA, Cohen RA, Colucci WS (2010) Oxidative posttranslational modifications mediate decreased SERCA activity and myocyte dysfunction in Galphaq-overexpressing mice. Circ Res 107(2):228–232
77. Levine RJ, Kensler RW, Yang Z, Stull JT, Sweeney HL (1996) Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments. Biophys J 71(2):898–907
78. Levine RJ, Yang Z, Epstein ND, Fananapazir L, Stull JT, Sweeney HL (1998) Structural and functional responses of mammalian thick filaments to alterations in myosin regulatory light chains. J Struct Biol 122(1–2):149–161
79. LeWinter MM, Granzier H (2010) Cardiac titin: a multifunctional giant. Circulation 121(19):2137–2145
80. Little SC, Biesiadecki BJ, Kilic A, Higgins RS, Janssen PM, Davis JP (2012) The rates of Ca2+ dissociation and cross-bridge detachment from ventricular myofibrils as reported by a fluorescent cardiac troponin C. J Biol Chem 287(33):27930–27940
81. Liu B, Tikunova SB, Kline KP, Siddiqui JK, Davis JP (2012) Disease-related cardiac troponins alter thin filament Ca2+ association and dissociation rates. PLoS ONE 7(6):e38259
82. Liu B, Lopez JJ, Biesiadecki BJ, Davis JP (2014) Protein kinase C phosphomimetics alter thin filament ca(2+) binding properties. PLoS ONE 9(1):e86279
83. Luers C, Fialka F, Elgner A, Zhu D, Kockskamper J, Von Lewinski D, Pieske B (2005) Stretch-dependent modulation of [Na+]i, [Ca2+]i, and pHi in rabbit myocardium–a mechanism for the slow force response. Cardiovasc Res 68:454–463
84. Luther PK, Bennett PM, Knupp C, Craig R, Padron R, Harris SP, Patel J, Moss RL (2008) 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 384(1):60–72
85. MacLennan DH, Kranias EG (2003) Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4(7):566–577
86. Mak A, Smillie LB, Barany M (1978) Specific phosphorylation at serine-283 of alpha tropomyosin from frog skeletal and rabbit skeletal and cardiac muscle. Proc Natl Acad Sci USA 75(8):3588–3592
87. Mateja RD, de Tombe PP (2012) Myofilament length-dependent activation develops within 5 ms in guinea-pig myocardium. Biophys J 103(1):L13–15
88. McDonald KS (2011) The interdependence of Ca2+ activation, sarcomere length, and power output in the heart. Pflugers Arch 462(1):61–67
89. McDonough JL, Arrell DK, Van Eyk JE (1999) Troponin I degradation and covalent complex formation accompanies myocardial ischemia/reperfusion injury. Circ Res 84(1):9–20
90. Metzger JM, Greaser ML, Moss RL (1989) Variations in cross-bridge attachment rate and tension with phosphorylation of myosin in mammalian skinned skeletal muscle fibers. Implications for twitch potentiation in intact muscle. J Gen Physiol 93(5):855–883
91. Milani-Nejad N, Janssen PM (2014) Small and large animal models in cardiac contraction research: advantages and disadvantages. Pharmacol Ther 141(3):235–249
92. Milani-Nejad N, Xu Y, Davis JP, Campbell KS, Janssen PM (2013) Effect of muscle length on cross-bridge kinetics in intact cardiac trabeculae at body temperature. J Gen Physiol 141(1):133–139
93. Monasky MM, Varian KD, Davis JP, Janssen PML (2008) Dissociation of force decline from calcium decline by preload in isolated rabbit myocardium. Pflugers Arch 456(2):267–276
94. Monasky MM, Biesiadecki BJ, Janssen PM (2010) Increased phosphorylation of tropomyosin, troponin I, and myosin light chain-2 after stretch in rabbit ventricular myocardium under physiological conditions. J Mol Cell Cardiol 48(5):1023–1028
95. Monasky MM, Taglieri DM, Jacobson AK, Haizlip KM, Solaro RJ, Janssen PM (2013) Post-translational modifications of myofilament proteins involved in length-dependent prolongation of relaxation in rabbit right ventricular myocardium. Arch Biochem Biophys 535(1):22–29
96. Moravec CS, Desnoyer RW, Milovanovic M, Schluchter MD, Bond M (1997) Mitochondrial calcium content in isolated perfused heart: effects of inotropic stimulation. Am J Physiol 273(3 Pt 2):H1432–1439
97. Morris TE, Sulakhe PV (1997) Sarcoplasmic reticulum Ca(2+)-pump dysfunction in rat cardiomyocytes briefly exposed to hydroxyl radicals. Free Radic Biol Med 22(1–2):37–47
98. Narolska NA, Piroddi N, Belus A, Boontje NM, Scellini B, Deppermann S, Zaremba R, Musters RJ, dos Remedios C, Jaquet K, Foster DB, Murphy AM, van Eyk JE, Tesi C, Poggesi C, van der Velden J, Stienen GJ (2006) Impaired diastolic function after exchange of endogenous troponin I with C-terminal truncated troponin I in human cardiac muscle. Circ Res 99(9):1012–1020
99. Nixon BR, Thawornkaiwong A, Jin J, Brundage EA, Little SC, Davis JP, Solaro RJ, Biesiadecki BJ (2012) AMP-activated protein kinase phosphorylates cardiac troponin I at Ser-150 to increase myofilament calcium sensitivity and blunt PKA-dependent function. J Biol Chem 287(23):19136–19147
100. Nixon BR, Liu B, Scellini B, Tesi C, Piroddi N, Ogut O, Solaro RJ, Ziolo MT, Janssen PM, Davis JP, Poggesi C, Biesiadecki BJ (2013) Tropomyosin Ser-283 pseudo-phosphorylation slows myofibril relaxation. Arch Biochem Biophys 535(1):30–38
101. Nixon BR, Walton SD, Zhang B, Brundage EA, Little SC, Ziolo MT, Davis JP, Biesiadecki BJ (2014) Combined troponin I Ser-150 and Ser-23/24 phosphorylation sustains thin filament Ca2+ sensitivity and accelerates deactivation in an acidic environment. J Mol Cell Cardiol (in press)
102. Nyitrai M, Geeves MA (2004) Adenosine diphosphate and strain sensitivity in myosin motors. Philos Trans R Soc Lond B 359(1452):1867–1877
103. Oceandy D, Stanley PJ, Cartwright EJ, Neyses L (2007) The regulatory function of plasma-membrane Ca(2+)-ATPase (PMCA) in the heart. Biochem Soc Trans 35(Pt 5):927–930
104. Olsson MC, Patel JR, Fitzsimons DP, Walker JW, Moss RL (2004) Basal myosin light chain phosphorylation is a determinant of Ca2+ sensitivity of force and activation dependence of the kinetics of myocardial force development. Am J Physiol Heart Circ Physiol 287(6):H2712–2718
105. Ottolia M, Philipson KD (2013) NCX1: mechanism of transport. Adv Exp Med Biol 961:49–54
106. Palmer BM, Georgakopoulos D, Janssen PM, Wang Y, Alpert NR, Belardi DF, Harris SP, Moss RL, Burgon PG, Seidman CE, Seidman JG, Maughan DW, Kass DA (2004) Role of cardiac myosin binding protein C in sustaining left ventricular systolic stiffening. Circ Res 94(9):1249–1255
107. Palmiter KA, Tyska MJ, Dupuis DE, Alpert NR, Warshaw DM (1999) Kinetic differences at the single molecule level account for the functional diversity of rabbit cardiac myosin isoforms. J Physiol 519(Pt 3):669–678
108. Pan BS, Solaro RJ (1987) Calcium-binding properties of troponin C in detergent-skinned heart muscle fibers. J Biol Chem 262(16):7839–7849
109. Patel JR, Diffee GM, Huang XP, Moss RL (1998) Phosphorylation of myosin regulatory light chain eliminates force-dependent changes in relaxation rates in skeletal muscle. Biophys J 74(1):360–368
110. Pena JR, Wolska BM (2004) Troponin I phosphorylation plays an important role in the relaxant effect of beta-adrenergic stimulation in mouse hearts. Cardiovasc Res 61(4):756–763
111. Perchenet L, Hinde AK, Patel KC, Hancox JC, Levi AJ (2000) Stimulation of Na/Ca exchange by the beta-adrenergic/protein kinase A pathway in guinea-pig ventricular myocytes at 37 degrees C. Pflugers Arch 439(6):822–828
112. Perry SV (1999) Troponin I: inhibitor or facilitator. Mol Cell Biochem 190(1–2):9–32
113. Piacentino V 3rd, Weber CR, Chen X, Weisser-Thomas J, Margulies KB, Bers DM, Houser SR (2003) Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circ Res 92(6):651–658
114. Piroddi N, Belus A, Scellini B, Tesi C, Giunti G, Cerbai E, Mugelli A, Poggesi C (2007) Tension generation and relaxation in single myofibrils from human atrial and ventricular myocardium. Pflugers Arch 454(1):63–73
115. Puglisi JL, Bassani RA, Bassani JW, Amin JN, Bers DM (1996) Temperature and relative contributions of Ca transport systems in cardiac myocyte relaxation. Am J Physiol 270(5 Pt 2):H1772–1778
116. Ramirez-Correa GA, Jin W, Wang Z, Zhong X, Gao WD, Dias WB, Vecoli C, Hart GW, Murphy AM (2008) O-linked GlcNAc modification of cardiac myofilament proteins: a novel regulator of myocardial contractile function. Circ Res 103(12):1354–1358
117. Reeves JP, Bailey CA, Hale CC (1986) Redox modification of sodium-calcium exchange activity in cardiac sarcolemmal vesicles. J Biol Chem 261(11):4948–4955
118. Rice JJ, Winslow RL, Hunter WC (1999) Comparison of putative cooperative mechanisms in cardiac muscle: length dependence and dynamic responses. Am J Physiol 276(5 Pt 2):H1734–1754
119. Rice R, Guinto P, Dowell-Martino C, He H, Hoyer K, Krenz M, Robbins J, Ingwall JS, Tardiff JC (2010) Cardiac myosin heavy chain isoform exchange alters the phenotype of cTnT-related cardiomyopathies in mouse hearts. J Mol Cell Cardiol 48(5):979–988
120. Roof SR, Shannon TR, Janssen PM, Ziolo MT (2011) Effects of increased systolic Ca2+ and phospholamban phosphorylation during {beta}-adrenergic stimulation on Ca2+ transient kinetics in cardiac myocytes. Am J Physiol Heart Circ Physiol 301(4):H1570–1578
121. Roof SR, Biesiadecki BJ, Davis JP, Janssen PM, Ziolo MT (2012) Effects of increased systolic Ca(2+) and beta-adrenergic stimulation on Ca(2+) transient decline in NOS1 knockout cardiac myocytes. Nitric Oxide 27(4):242–247
122. Sadayappan S, Osinska H, Klevitsky R, Lorenz JN, Sargent M, Molkentin JD, Seidman CE, Seidman JG, Robbins J (2006) Cardiac myosin binding protein C phosphorylation is cardioprotective. Proc Natl Acad Sci USA 103(45):16918–16923
123. Scherer NM, Deamer DW (1986) Oxidative stress impairs the function of sarcoplasmic reticulum by oxidation of sulfhydryl groups in the Ca2 + −ATPase. Arch Biochem Biophys 246(2):589–601
124. Siemankowski RF, Wiseman MO, White HD (1985) ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc Natl Acad Sci USA 82(3):658–662
125. Simnett SJ, Johns EC, Lipscomb S, Mulligan IP, Ashley CC (1998) Effect of pH, phosphate, and ADP on relaxation of myocardium after photolysis of diazo 2. Am J Physiol 275(3 Pt 2):H951–960
126. Sivakumaran V, Stanley BA, Tocchetti CG, Ballin JD, Caceres V, Zhou L, Keceli G, Rainer PP, Lee DI, Huke S, Ziolo MT, Kranias EG, Toscano JP, Wilson GM, O’Rourke B, Kass DA, Mahaney JE, Paolocci N (2013) HNO Enhances SERCA2a Activity and Cardiomyocyte Function by Promoting Redox-Dependent Phospholamban Oligomerization. Antioxid Redox Signal 19(11):1185–1197
127. Slabaugh JL, Brunello L, Gyorke S, Janssen PM (2012) Contractile parameters and occurrence of alternans in isolated rat myocardium at supra-physiological stimulation frequency. Am J Physiol Heart Circ Physiol 302(11):H2267–2275
128. Solaro RJ (2001) Modulation of cardiac Myofilament activity by protein phosphorylation. In: Page E, Fozzard H, Solaro RJ (eds) Handbook of Physiology: Section 2, vol 1, The Cardiovascular System. Oxford University Press, New York, pp 264–300
129. Solaro RJ, Westfall M (2005) Physiology of the myocardium. In: Sellke FW (ed) Surgery of the Chest. Elsevier Sanders, Philadelphia, pp 767–779
130. Starling EH (1918) The Lineacre lecture on the law of the heart. Longmans Green, London
131. Stehle R, Iorga B (2010) Kinetics of cardiac sarcomeric processes and rate-limiting steps in contraction and relaxation. J Mol Cell Cardiol 48(5):843–850
132. Stelzer JE, Moss RL (2006) Contributions of stretch activation to length-dependent contraction in murine myocardium. J Gen Physiol 128(4):461–471
133. Stelzer JE, Patel JR, Walker JW, Moss RL (2007) Differential roles of cardiac myosin-binding protein C and cardiac troponin I in the myofibrillar force responses to protein kinase A phosphorylation. Circ Res 101(5):503–511
134. Strang KT, Sweitzer NK, Greaser ML, Moss RL (1994) Beta-adrenergic receptor stimulation increases unloaded shortening velocity of skinned single ventricular myocytes from rats. Circ Res 74(3):542–549
135. Sumandea MP, Pyle WG, Kobayashi T, de Tombe PP, Solaro RJ (2003) Identification of a functionally critical protein kinase C phosphorylation residue of cardiac troponin T. J Biol Chem 278(37):35135–35144
136. Suzuki T, Palmer BM, James J, Wang Y, Chen Z, VanBuren P, Maughan DW, Robbins J, LeWinter MM (2009) Effects of cardiac myosin isoform variation on myofilament function and crossbridge kinetics in transgenic rabbits. Circ Heart Fail 2(4):334–341
137. Szczesna D (2003) Regulatory light chains of striated muscle myosin. Structure, function and malfunction. Curr Drug Targets Cardiovasc Haematol Disord 3(2):187–197
138. Takagi Y, Homsher EE, Goldman YE, Shuman H (2006) Force generation in single conventional actomyosin complexes under high dynamic load. Biophys J 90(4):1295–1307
139. Takimoto E, Soergel DG, Janssen PM, Stull LB, Kass DA, Murphy AM (2004) Frequency- and afterload-dependent cardiac modulation in vivo by troponin I with constitutively active protein kinase A phosphorylation sites. Circ Res 94(4):496–504
140. Tardiff JC (2011) Thin filament mutations: developing an integrative approach to a complex disorder. Circ Res 108(6):765–782
141. ter Keurs HE, Rijnsburger WH, van Heuningen R, Nagelsmit MJ (1980) Tension development and sarcomere length in rat cardiac trabeculae, Evidence of length-dependent activation. Circ Res 46(5):703–714
142. Tong CW, Gaffin RD, Zawieja DC, Muthuchamy M (2004) Roles of phosphorylation of myosin binding protein-C and troponin I in mouse cardiac muscle twitch dynamics. J Physiol 558 (0022–3751 (Print)):927–941.
143. 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(9):974–982
144. Torres CAA, Varian KD, Janssen PML (2008) Variability in interbeat duration influences myocardial contractility in rat cardaic trabeculae. Open Cardiovasc Med J 2:96–100
145. Turnbull L, Hoh JF, Ludowyke RI, Rossmanith GH (2002) Troponin I phosphorylation enhances crossbridge kinetics during beta-adrenergic stimulation in rat cardiac tissue. J Physiol 542(Pt 3):911–920
146. van der Velden J, Papp Z, Boontje NM, Zaremba R, de Jong JW, Janssen PM, Hasenfuss G, Stienen GJ (2003) The effect of myosin light chain 2 dephosphorylation on Ca2 + − sensitivity of force is enhanced in failing human hearts. Cardiovasc Res 57(2):505–514
147. Varian KD, Janssen PML (2007) Frequency-dependent acceleration of relaxation involves decreased myofilament calcium sensitivity. Am J Physiol Heart Circ Physiol 292(5):H2212–2219
148. Varian KD, Kijtawornrat A, Gupta SC, Torres CA, Monasky MM, Hiranandani N, Delfin DA, Rafael-Fortney JA, Periasamy M, Hamlin RL, Janssen PML (2009) Impairment of diastolic function by lack of frequency-dependent myofilament desensitization rabbit right ventricular hypertrophy. Circ Heart Fail 2(5):472–481
149. Waggoner JR, Ginsburg KS, Mitton B, Haghighi K, Robbins J, Bers DM, Kranias EG (2009) Phospholamban overexpression in rabbit ventricular myocytes does not alter sarcoplasmic reticulum Ca transport. Am J Physiol Heart Circ Physiol 296(3):H698–703
150. Walker LA, Medway AM, Walker JS, Cleveland JC Jr, Buttrick PM (2011) Tissue procurement strategies affect the protein biochemistry of human heart samples. J Muscle Res Cell Motil 31(5–6):309–314
151. Wang H, Kohr MJ, Traynham CJ, Wheeler DG, Janssen PM, Ziolo MT (2008) Neuronal nitric oxide synthase signaling within cardiac myocytes targets phospholamban. Am J Physiol Cell Physiol 294(6):C1566–1575
152. Weisberg A, Winegrad S (1996) Alteration of myosin cross bridges by phosphorylation of myosin-binding protein C in cardiac muscle. Proc Natl Acad Sci USA 93(17):8999–9003
153. Westerblad H, Allen DG (1993) The influence of intracellular pH on contraction, relaxation and [Ca2+]i in intact single fibres from mouse muscle. J Physiol 466:611–628
154. Wijnker PJ, Sequeira V, Foster DB, Li Y, Dos Remedios CG, Murphy AM, Stienen GJ, van der Velden J (2014) Length-dependent activation is modulated by cardiac troponin-I biphosphorylation at Ser23 and Ser24 but not by Thr143 phosphorylation. Am J Physiol Heart Circ Physiol 306:H1171–H1181
155. Williams GS, Boyman L, Chikando AC, Khairallah RJ, Lederer WJ (2013) Mitochondrial calcium uptake. Proc Natl Acad Sci USA 110(26):10479–10486
156. Wu Y, Bell SP, Trombitas K, Witt CC, Labeit S, LeWinter MM, Granzier H (2002) Changes in titin isoform expression in pacing-induced cardiac failure give rise to increased passive muscle stiffness. Circulation 106(11):1384–1389
157. Xu KY, Zweier JL, Becker LC (1997) Hydroxyl radical inhibits sarcoplasmic reticulum Ca(2+)-ATPase function by direct attack on the ATP binding site. Circ Res 80(1):76–81
158. 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(11):1181–1188
159. Yasuda S, Coutu P, Sadayappan S, Robbins J, Metzger JM (2007) Cardiac transgenic and gene transfer strategies converge to support an important role for troponin I in regulating relaxation in cardiac myocytes. Circ Res 101(4):377–386
160. Yuan C, Guo Y, Ravi R, Przyklenk K, Shilkofski N, Diez R, Cole RN, Murphy AM (2006) Myosin binding protein C is differentially phosphorylated upon myocardial stunning in canine and rat hearts– evidence for novel phosphorylation sites. Proteomics 6(14):4176–4186
161. Yuan C, Sheng Q, Tang H, Li Y, Zeng R, Solaro RJ (2008) Quantitative comparison of sarcomeric phosphoproteomes of neonatal and adult rat hearts. Am J Physiol Heart Circ Physiol 295(2):H647–656
162. Zhang R, Zhao J, Mandveno A, Potter JD (1995) Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation. Circ Res 76(6):1028–1035
163. Zhang P, Kirk JA, Ji W, dos Remedios CG, Kass DA, Van Eyk JE, Murphy AM (2012) Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart. Circulation 126(15):1828–1837
164. Ziolo MT, Maier LS, Piacentino V 3rd, Bossuyt J, Houser SR, Bers DM (2004) Myocyte nitric oxide synthase 2 contributes to blunted beta-adrenergic response in failing human hearts by decreasing Ca2+ transients. Circulation 109(15):1886–1891